Activity and exploratory behavior of adult offspring of undernourished mother rats

Mother rats were either adequately fed or were undernourished during much of pregnancy and throughout lactation. Both control (C) and undernourished (UN) offspring had free access to food from weaning. Rats were tested between 15 and 27 weeks of age. During repeated exposures on the same day in a rectangular observation box, UN rats moved about more and reared on their hind legs more often than controls, but defecated less frequently. Two measures of exploratory behavior, tendency to emerge from a familiar to an unfamiliar area and responsiveness to a novel object, did not differentiate the 2 groups, nor did control and UN rats differ in the rate at which they pressed a lever to produce a light stimulus in a dark Skinner box. These and other long-term, activity studies indicate that previously undernourished rats are more active than controls in familiar, nonstressful situations.     

Contribution of amygdalar and lateral hypothalamic neurons to visual information processing of food and nonfood in monkey

Visual information processing was investigated in the inferotemporal cortical (ITCx)-amygdalar (AM)-lateral hypothalamic (LHA) axis which contributes to food-nonfood discrimination. Neuronal activity was recorded from monkey AM and LHA during discrimination of sensory stimuli including sight of food or nonfood. The task had four phases: control, visual, bar press, and ingestion. Of 710 AM neurons tested, 220 (31.0%) responded during visual phase: 48 to only visual stimulation, 13 (1.9%) to visual plus oral sensory stimulation, 142 (20.0%) to multimodal stimulation and 17 (2.4%) to one affectively significant item. Of 669 LHA neurons tested, 106 (15.8%) responded in the visual phase. Of 80 visual-related neurons tested systematically, 33 (41.2%) responded selectively to the sight of any object predicting the availability of reward, and 47 (58.8%) responded nondifferentially to both food and nonfood. Many of AM neuron responses were graded according to the degree of affective significance of sensory stimuli (sensory-affective association), but responses of LHA food responsive neurons did not depend on the kind of reward indicated by the sensory stimuli (stimulus-reinforcement association). Some AM and LHA food responses were modulated by extinction or reversal. Dynamic information processing in ITCx-AM-LHA axis was investigated by reversible deficits of bilateral ITCx or AM by cooling. ITCx cooling suppressed discrimination by vision responding AM neurons (8/17). AM cooling suppressed LHA responses to food (9/22). We suggest deep AM-LHA involvement in food-nonfood discrimination based on AM sensory-affective association and LHA stimulus-reinforcement association.     

Rats exposed to traumatic stress bury unfamiliar objects--a novel measure of hyper-vigilance in PTSD models?

Electric shocks lead to lasting behavioral deficits in rodents, and as such are often used to model post-traumatic stress disorder (PTSD) in the laboratory. Here we show that a single exposure of rats to 3 mA-strong shocks results in a marked social avoidance that lasts at least 28 days; moreover, the response intensifies over time. In an attempt to study the impact of cue reminders on the behavior of shocked rats, we administered shocks in the presence of a highly conspicuous, 10 cm-large object. This object was introduced into the home cage of rats 28 days after shock exposure. Shocked rats manipulated the object considerably less than controls. More importantly, however, the object was buried by shocked rats. This behavior was virtually absent in controls. The response strongly depended on the intensity of shocks, and was robust. Rats shocked with 3 mA currents spent 40% of time burying the object, which was often hardly visible at the end of the 5 min test. Subsequent experiments demonstrated that the response was not cue-specific as unfamiliar objects were also buried. Rats are well known to bury dangerous objects; the shock-prod burying test of anxiety is based on this response. Behavioral similarities with this test and the differences from the marble-burying behavior of mice suggest that traumatized rats bury unfamiliar objects in defense, and the response can be interpreted as a sign of hyper-vigilance. We further suggest that object burying can be used as a sign of hyper-vigilance in models of PTSD.     

Emergence of the exploratory motive in rats

As infant rats approach weaning, they must overcome their infantile attraction to the home nest and prepare to leave its safety to forage for food. Although nutritive needs may help to motivate pups to make this bold move, a newly emerging exploratory motive also may play a role. Three experiments are reported here which examine age-related changes in the exploratory motive. In the first experiment, preferences for a novel side over a familiar side of a two-sided testing chamber were examined in postnatal Days 15 (P15), 17 (P17), 19 (P19), and 21 (P21) rat pups. Subjects did not prefer to explore the novel side until P19. In the same test, no preference for a novel object was observed at any of the ages tested, suggesting that this preference, which is expressed in adulthood, does not emerge until a later age; however, additional studies are needed to verify this. In the second experiment, P15 subjects demonstrated their ability to discriminate the two sides of the testing chamber in a novelty-induced locomotion test. In the third experiment, the presence of a home-nest-associated object was shown to inhibit exploration of novel context in P15, but not P21, subjects. These data suggest that home nest egression may be more the consequence of the declining attractiveness of the home nest than of a growing exploratory motive.     

Long-term object location memory in rats: Effects of sample phase and delay length in spontaneous place recognition test

This study investigates the effects of sample phase and delay length on discrimination performance in the spontaneous place recognition (SPR) test in rats. Rats were allowed to explore an arena where two identical objects were presented for 5–20 min (sample phase). After a delay interval, rats were placed again in the same arena but one of the two objects was moved to a novel place (test phase). Results showed that when the sample phase was as long as 20 min, rats preferentially explored the moved object during the test phase even after a 6–24 h delay was interposed. Further sequential and cumulative analyses of the test phase revealed that the preference for the object in a novel place was evident in the first and 2nd min of the test phase in rats with a longer sample phase duration. Correlation analysis showed that locomotor activity and object exploration in the sample phase were not decisive factors in spatial memory performance. The present results demonstrate the importance of the sample phase exposure time and the test phase length.     

Age-associated deficits in pattern separation functions of the perirhinal cortex: a cross-species consensus

Normal aging causes a decline in object recognition. Importantly, lesions of the perirhinal cortex produce similar deficits and also lead to object discrimination impairments when the test objects share common features, suggesting that the perirhinal cortex participates in perceptual discrimination. The current experiments investigated the ability of young and aged animals to distinguish between objects that shared features with tasks with limited mnemonic demands. In the first experiment, young and old rats performed a variant of the spontaneous object recognition task in which there was a minimal delay between the sample and the test phase. When the test objects did not share any features ("Easy" perceptual discrimination) both young and aged rats correctly identified the novel object. When the test objects contained overlapping features, however, only the young rats showed an exploratory preference for the novel object. In Experiment 2, young and aged monkeys were tested on an object discrimination task. When the object pairs were dissimilar, both the young and aged monkeys learned to select the rewarded object quickly. In contrast, when LEGOs? were used to create object pairs with overlapping features, the aged monkeys took significantly longer than did the young animals to learn to discriminate between the rewarded and the unrewarded object. Together, these data indicate that behaviors requiring the perirhinal cortex are disrupted in advanced age, and suggest that at least some of these impairments may be explained by changes in high-level perceptual processing in advanced age.     

Neonatal 192 IgG-saporin lesions of basal forebrain cholinergic neurons selectively impair response to spatial novelty in adult rats

The role of the developing cholinergic basal forebrain system on cognitive behaviors was examined in 7 day-old rats by giving lesions with intraventricular injections of 192 IgG-saporin or saline. Rats were subjected to passive avoidance on postnatal days (PND) 22-23, water maze testing on PND 50-60, and a open-field test (in which reactions to spatial and object novelty were measured) on PND 54. Behavioral effects of the lesions were evident only in the open-field test with 5 objects. Unlike controls, the lesioned rats did not detect a spatial change after a displacement of 2 of the 5 objects. Control and lesioned rats, however, showed comparable novelty responses to an unfamiliar object. Lesion effectiveness was confirmed by 75% and 84% decreases in choline acetyltransferase activity in cortex and hippocampus. These results suggest that the developing cholinergic system may be involved in spatial information processing or attention to spatial modifications.     

Ontogeny of spatial discrimination in mice: a longitudinal analysis in the modified open-field with objects

The present longitudinal study investigated the emergence of spatial discrimination and reaction to novelty in CD-1 mice, using a modified open-field test with four objects, a test in which responses to both spatial rearrangement of familiar objects and object novelty are assessed. Male and female mice were tested on postnatal days (pnd) 18, 28, 46 and 90. Locomotor activity was highest on pnd 90, whereas time spent on objects before rearrangement was highest on pnd 46. Eighteen-day old mice were unable to detect both object rearrangement and object novelty, suggesting immaturity in processing spatial information. On days 28 and 46 mice showed a clear response to object novelty, actively exploring the unfamiliar object placed in the arena, while at these ages object displacement elicited a generalized increase of exploration, not directed towards the displaced objects. A clear and selective response to object displacement emerged only at adulthood (day 90).     

Object discrimination by rats: The role of frontal and hippocampal systems in retention and reversal

The present experiment was designed to determine whether the reversal deficit in nonspatial discrimination tasks following frontal or hippocampal system damage was a result of the spatial components of those tasks, or a general reversal deficit. Rats were trained to choose between two objects based on the stimulus characteristics of the objects themselves; neither the absolute location of the objects in the test arena nor the position of the objects with respect to the rat accurately predicted the correct choice. Rats with either frontal cortex or fimbria-fornix lesions performed worse than controls in both postoperative retention and reversal of the object discrimination. The performance of rats with frontal cortex damage was impaired during the first two postoperative reversals; but not during subsequent reversals. The performance of rats with fornix lesions was impaired only on the first postoperative reversal. These data demonstrate that the nonspatial reversal impairment following damage to either the frontal cortical or hippocampal systems is the result of a general reversal deficit, and is not due to the spatial components of nonspatial tasks.     

Factors affecting sucrose preference behavior in rats with hippocampal lesions

Rats with hippocampal lesions were compared to rats with neocortical lesions and to normal unoperated animals on tests of sucrose preference in both a short (5 min) and a long (24 hr) test session. Sucrose preference behavior was examined on a seven point solution range which extended from water to 48% sucrose. Rats with hippocampal lesions failed to show any preference for sucrose in the 5-min test session, whereas the same animals were identical to controls in the 24-hr test. Additional groups with comparable lesions were also compared on tests of sucrose preference under conditions of both food and water deprivation. The hippocampally-ablated animals showed none or a markedly attenuated preference for sucrose when water deprived. The same animals were identical to the control groups when sucrose preference was tested under food deprivation. Under both deprivation conditions, however, the rats with hippocampal lesions changed significantly more often between the members of the test solution pairs. No differences were found between the cortical and normal unoperated control groups.     

Effect of the number of high-fat and low-fat cues on food choice

This study examined the effects on food choice of increasing the number of healthy items available (fruit) and decreasing the number of unhealthy items available (candy bars). A similar choice, involving nonfood items, was also examined. Two hundred eighty-nine men and women were randomly assigned to 1 of 4 experimental groups: (a) control group, (b) increased number of fruits, (c) decreased number of candy bars, and (d) combination. Between 30% and 40% of participants chose fruit regardless of the amount of fruit and candy presented: there was no effect of increasing fruit or decreasing candy bars. However, restrained participants and current dieters were more likely to choose fruit. In contrast, both stimulus control techniques were effective in increasing the percentage of participants choosing a nonfood item. These results suggest that stimulus control may not be sufficient to modify food choice: other powerful factors affect eating behavior, and these must be considered.     

Mirror neurons and intention understanding: Dissociating the contribution of object type and intention to mirror responses using electromyography

Since their discovery in the monkey and human brain, mirror neurons have been claimed to play a key role in understanding others' intentions. For example, “action‐constrained” mirror neurons in inferior parietal lobule fire when the monkey observes a grasping movement that is followed by an eating action, but not when it is followed by a placing action. It is claimed these responses enable the monkey to predict the intentions of the actor. These findings have been replicated in human observers by recording electromyography responses of the mouth‐opening mylohyoid muscle during action observation. Mylohyoid muscle activity was greater during the observation of actions performed with the intention to eat than of actions performed with the intention to place, again suggesting an ability to predict the actor's intentions. However, in previous studies, intention was confounded with object type (food for eating actions, nonfood for placing actions). We therefore used electromyography to measure mylohyoid activity in participants observing eating and placing actions. Unlike previous studies, we used a design in which each object (food, nonfood) could be both eaten and placed, and thus participants could not predict the actor's intention at the onset of the action. Greater mylohyoid activity was found for the observation of actions performed on food objects, irrespective of intention, indicating that the object type, not the actor's intention, drives the mirror response. This result suggests that observers' motor responses during action observation reflect the presence of a particular object, rather than the actor's underlying intentions.     

Exploratory behavior in mice selectively bred for developmental differences in aggressive behavior

The development and expression of exploratory behavior was assessed in the Cairns lines of Institute for Cancer Research (ICR) mice that were selectively bred for differences in aggressive behavior, with a high-aggressive 900 line, low-aggressive 100 line, and control 500 line. Four paradigms were employed. Developmental changes were evident in the complex novel arena, with older males faster to contact a novel object, and ambulating more than young males. Within the control 500 line, older males showed longer latency to emerge from the home cage, and shorter latency to contact novel objects. In the 900 line, younger males showed this same pattern. R. B. Cairns proposed that line differences in aggressive behavior arise through alterations in developmental timing [Cairns et al. [1983] Life-span developmental psychology (Vol. 5). New York: Academic Press; Gariépy et al. [2001] Animal Behaviour 61: 933-947]. The early appearance of mature patterns of exploratory behavior in 900 line males supports this interpretation. The 900 line males also appear to be behaviorally inhibited in novel settings such as the light-dark box and the neohypophagia paradigm, compared to the 500 and 100 lines (Experiments 1, 2, and 4). Moreover, in the most complex apparatus, the novel arena, 900 line males were slowest to exit the home cage, and fastest to contact a novel object. The apparent contrast in these parameters of exploratory behavior is discussed in relation to T. C. Schneirla's [1965 Advances in the study of behavior (Vol. 1). New York: PN Academic] approach-withdrawal theory.     

Allocation of attentional resources during habituation to food cues

Two experiments were designed to test the hypothesis that habituation to repeated food cues can be inhibited by allocating processing resources to nonfood cues. In two experiments, the salivary response to 10 presentations of lemon yogurt was assessed while subjects engaged in a controlled cognitive search task (demanding attentional resources), an automatic search task (needing fewer attentional resources), or no task. In Experiment 1, the controlled and automatic search tasks differed in the number of memory set items. In Experiment 2, the size of the memory sets was held constant, and individuals were provided practice to stabilize the different search strategies in the task. The automatic search and no task groups habituated to the repeated presentation of food cues in both experiments, but the controlled search group did not. These results support the hypothesis that allocation of attentional resources to external cues can influence the processing of food cues.     

Cholinergic blockade effects on spatial integration versus cue discrimination performance

A within-subjects investigation was conducted to determine the effects of central versus peripheral cholinergic blockade in animals tested either on a spatial integration task in which the possibility of rule learning was also available or on a visual discrimination task in which the daily location of food was marked by a distinctive visual stimulus pattern. All testing was conducted on the Maier three-table apparatus. It was found that the only effect of the peripheral cholinergic blockade on the performance of either task group was to produce a decrease in exploratory behavior. In contrast, central cholinergic blockade markedly impaired spatial integration performance; however, it did not impair the ability of animals in rule learning or visual discrimination learning. It was also found that central cholinergic blockade impaired the animal's tendency to enter all tables before reentering a given table during the exploratory phase of the daily session. This finding was interpreted as reflecting an impairment of working memory for spatial information, rather than a general impairment in working memory, and this interpretation was applied to the explanation of the deficit in the spatial integration performance.     

Presence of conspecifics facilitates learning that food is inedible in Aplysia fasciata.

The absence of a conspecific, but not of food, interfered with learning and memory of a feeding task in Aplysia fasciata. Interference was shown by a shortened training session and by lack of savings on retraining. The shortened training is not responsible for the lack of savings because brief training in the presence of a conspecific led to savings on retraining. Animals trained in the absence of a conspecific and then tested in its presence did not show signs of having learned, which indicates that the absence of a conspecific interfered with the ability to learn, rather than with the expression of memory. Absence of a conspecific also inhibited other aspects of feeding behavior, such as the latency to respond to food and the length of time that animals respond to food, which indicate that interference with learning was apparently caused by inhibition of feeding behavior, rather than by block of the mechanisms underlying learning.     

Self-stimulation and suppression of feeding observed at the same site in the amygdala

Rats with electrodes implanted bilaterally in the amygdala were allowed to bar-press for bilateral stimulation. The same stimulation suppressed feeding, and the degree of suppression observed was greater in the rats that exhibited bar-pressing than in a group that had not exhibited that behavior. The stimulation suppressed feeding when the animals were food deprived and when they were in a relatively satiated state. When the delivery of amygdaloid stimulation was made contingent on the animals' contact with the food their rate of contact was increased, but their rate of feeding was decreased compared to normal values. The possibility that suppression was related to the elicitation of exploratory behavior by amygdaloid stimulation was discussed.     

Effects of acute food and/or water deprivation on muricide

The present experiment was designed to test certain predictions derived from models of interactions between muricide and appetitive behaviors proposed earlier by Russell and Singer [8,9]. One of the major features of the models centered on whether the two types of behavior are inevitably related. The general design of the present experiment involved testing for muricide either (a) after deprivation of food and/or water or (b) at times during the normal diurnal cycle when the two consummatory responses were at their minima and maxima. Deprivation and testing for muricide were limited to a single episode in order to eliminate confounding effects of repeated deprivations and of repeated exposures to prey. Periods of acute deprivation ranging from 5.5 to 22.0 hr did not induce significant quantitative changes in muricidal behavior. However, muricide and the appetitive behaviors did co-vary under conditions associated with the normal diurnal cycle. Comparing the present results with findings from experiments using repeated deprivation leads to the suggestion that covariation of appetitive and muricidal behaviors is not an innate characteristic, but rather is acquired through processes of learning. Present results further suggest that each of the two types of behavior has its own physiological substrate which can be modified independently, but also may be activated concomitantly by a common set of antecedent conditions.     

Object exploration in the developing rat: Methodological considerations

The current study was conducted to characterize the ontogeny of novel object recognition in rats. Initial testing (Experiment 1) was conducted in a square arena and it was observed that 21‐day‐old animals would often pause in the corners, greatly increasing between‐subject variability and performance in this test. Significantly greater object exploration and less variability were obtained using a circular arena. In Experiment 2, we report object exploration in 21, 35, 42, and 90‐day‐old male and female Sprague‐Dawley rats using a circular arena. The results show that measures of locomotor activity, object exploration, and within session habituation of these behaviors were surprisingly similar across all ages. Gender differences in locomotor activity were not observed until 42 days of age. Reliable recognition memory was observed at all ages. It is concluded that the novel object recognition test appears well suited for use in young rats. © 2012 Wiley Periodicals, Inc. Dev Psychobiol 55: 373–381, 2013     

Hypothalamic influences on sensory reinforcement.

Rats were tested in a darkened chamber containing two levers, one of which turned on a dim light when depressed. Rats receiving non-contingent electrical stimulation of the lateral hypothalamus made many more lever presses than did unstimulated controls and made more presses on the light producing lever than on the inactive one. Pretests had shown that the electrical stimulation elicited consummatory behavior in the presence of appropriate goal objects. Dynamic hyperphagic rats maintained on a restricted diet made more total responses early in testing than did their controls which also received the same restricted diet. They also preferred the light producing lever, but not reliably more than did their controls. Static hyperphagic rats made fewer total responses than did their controls, both groups receiving food ad lib. Neither group showed any preference between the two levers.