The role of environmental familiarization in novel-object preference

The experiments in this report examined the behavioral variables modulating novel-object preference in a widely used 'object recognition' preparation. This preparation takes advantage of the tendency of rats to interact more with a novel than a familiar 'sample' object in a free-choice situation. Experiment 1 examined the interaction between environmental familiarization and the duration of sample-object exposure in the development of a novel-object preference. Interaction with the sample object during sample-object exposure was increased when rats were given time in the environment prior to presentation of the sample object. Also, provided that the sample-object exposure was greater than 2 min, rats given environmental familiarization time prior to sample-object exposure displayed a novel-object preference. Rats that received the same amount of sample-object exposure without prior exposure to the environment alone did not discriminate between the sample and novel object. In Experiments 2 and 3, sample-object exposure occurred in a different environment than the novel-object test. Novel-object preference was not affected regardless of whether that testing environment was familiar or novel. This result differs from previous work that finds that an object recovers some novelty when moved to a new spatial location.     

Prenatal and early sucking influences on dietary preference in newborn, weaning, and young adult cats

Early experiences are of potential importance in shaping long-term behavior. This study examined the relative influence of prenatal and/or early postnatal experience of chemosensory stimuli on subsequent olfactory and dietary preferences of cats as newborns, at 9-10 weeks, and at 6 months. Cats were exposed to vanillin or 4-ethylguaiacol via their mother's diet either prenatally, postnatally, perinatally (prenatal and postnatal), or experienced no exposure to the stimuli (control). Newborns were given a two-choice olfactory test between the familiar "odor" and no odor; 9-10 week olds were tested for their preference between two food treats, one flavored with the familiar stimulus and the other unflavored; at 6 months, cats were given a choice of two bowls of food, one flavored with the familiar stimulus and the other unflavored. At all ages, cats preferred the familiar, and avoided the unfamiliar, stimulus. Perinatal exposure exerted the strongest influence on preference. Prenatal exposure influenced preference at all ages and postnatal exposure exerted a stronger effect as the cat aged. We conclude that long-term chemosensory and dietary preferences of cats are influenced by prenatal and early (nursing) postnatal experience, supporting a natural and biologically relevant mechanism for the safe transmission of diet from mother to young.     

Preferences for familiarity and novelty: a model for the simultaneous development of both

Many developing animals show an increasing preference for familiar companions and objects. They may also come to prefer things which are slightly different from the familiar. A model which shows how both processes can occur simultaneously is developed with particular reference to imprinting in birds. It shows how a biphasic curve would be obtained if preferences were measured in choice tests during the course of familiarization. The model predicts that shape of the preference curve will depend on the difference between the familiar and unfamiliar objects. It also predicts that the shape will be altered if inexperienced animals show a preference for one object over the other.     

Loss of shoaling preference for familiar individuals in captive-reared crimson spotted rainbowfish Melanotaenia duboulayi

Captive-reared rainbowfish Melanotonia duboulayi showed no preference for familiar individuals in an experiment examining shoaling preferences. Fortnightly re-examination of the shoaling preferences of the captive-reared population showed that the lack of preference for familiar individuals did not alter over an 8 week period. The same experiment performed on laboratory-reared offspring raised in isolated groups for 8 months since hatching also showed no preference for shoals consisting of familiar individuals. In contrast, trials performed on a wild population of M. duboulayi found a strong preference for familiar shoalmates, a result that is consistent with previous studies. The lack of shoaling preferences in captive-reared populations is probably the result of relaxed selection and inbreeding in the captive environment. The consequences of captive breeding for fish social behaviour are discussed with particular reference to hatchery production.     

Recognition memory in tree shrew (Tupaia belangeri) after repeated familiarization sessions

Recognition memories are formed during perceptual experience and allow subsequent recognition of previously encountered objects as well as their distinction from novel objects. As a consequence, novel objects are generally explored longer than familiar objects by many species. This novelty preference has been documented in rodents using the novel object recognition (NOR) test, as well is in primates including humans using preferential looking time paradigms. Here, we examine novelty preference using the NOR task in tree shrew, a small animal species that is considered to be an intermediary between rodents and primates. Our paradigm consisted of three phases: arena familiarization, object familiarization sessions with two identical objects in the arena and finally a test session following a 24-h retention period with a familiar and a novel object in the arena. We employed two different object familiarization durations: one and three sessions on consecutive days. After three object familiarization sessions, tree shrews exhibited robust preference for novel objects on the test day. This was accompanied by significant reduction in familiar object exploration time, occurring largely between the first and second day of object familiarization. By contrast, tree shrews did not show a significant preference for the novel object after a one-session object familiarization. Nonetheless, they spent significantly less time exploring the familiar object on the test day compared to the object familiarization day, indicating that they did maintain a memory trace for the familiar object. Our study revealed different time courses for familiar object habituation and emergence of novelty preference, suggesting that novelty preference is dependent on well-consolidated memory of the competing familiar object. Taken together, our results demonstrate robust novelty preference of tree shrews, in general similarity to previous findings in rodents and primates.     

Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience.

Prairie voles (Microtus ochrogaster) exhibit a monogamous mating system characterized by long-term pair bonds between mates. The purpose of this study was to examine the effect of cohabitation time and sexual experience on the development of pair bond formation in female prairie voles. Females that were allowed to cohabit for 24 hr or more, with or without mating, exhibited a strong social preference for a familiar partner versus a strange male. Females that cohabited and mated for 6 hr showed strong preferences for a familiar partner, while cohabitation for less than 24 hr, without mating, did not result in preferences for the familiar male. These results indicate that mating was not essential for partner preference formation; however, preferences developed more rapidly when mating occurred.     

Familiarity and partner preferences in female common voles, <Emphasis Type="Italic">Microtus arvalis</Emphasis>

Captive female common voles (Microtus arvalis) had a clear social preference for familiar males in a standard preference test. Cohabitation for a short period resulted in preferences for familiar partners, and females spent eight times more time in body contact with a familiar male than with an unfamiliar male. Females also displayed stranger-directed aggression. Our results suggest that the common vole is a species with selective partner preferences and a tendency to form tight social relationships and stable male–female associations.     

Development of visual species identification in ducklings: What is the role of imprinting?

The phenomenon of imprinting (a rapid form of exposure learning) is widely presumed to underlie the formation of normal, species-typical social preferences in precocial birds. To determine whether this is in fact the case, 24-h-old domestic and semi-wild mallard ducklings (Anas platyrhynchos) were allowed to follow a stuffed hen of one of three sympatric waterfowl species for 20 min. The models used were mallard, redhead (Aythya americana), and pintail (Anas acuta) hens. When later tested for their preference for the familiar hen in simultaneous choice tests with one of the other two stuffed models, only those birds trained with the Mallard and tested with the Mallard and Pintail models (designated the Mallard versus Pintail group) showed a preference for the familiar model. (That preference was shown by both domestic and semi-wild ducklings.) In none of the other three groups (Mallard versus Redhead, Redhead versus Mallard, and Pintail versus Mallard) was the imprinting procedure effective in producing a preference for the familiar model. When other ducklings were similarly trained with either the Mallard model, a red-and-white-striped box, or a green styrofoam ball, a preference for the familiar model was found in all four groups (Mallard versus Red Box, Red Box versus Mallard, Red Box versus Green Ball, and Green Ball versus Red Box). Increasing the length of the training period from 20 min to 2 h and to 24 h did not produce a preference for the familiar Mallard over the unfamiliar Redhead. These results raise some doubt that imprinting as currently conceived is the behavioural mechanism of visual species identification as it occurs in nature.     

Preferences for familiar fish do not vary with predation risk in the European minnow

In the near-natural conditions of a fluvarium in the River Frome, U.K., European minnows Phoxinus phoxinus displayed schooling preferences for familiar conspecifics. Schools were composed of 75% familiar fish. The minnows in this river co-occur with many piscivores, the most notable being the pike Esox Iucius . The preference for familiar shoalmates was not increased by the threat of predatory attack from a model pike, despite the antipredator benefits afforded to individual members of schools of familiar fish.     

Intra‐sexual preferences for familiar fish in male guppies

Male guppies Poecilia reticulata were observed to develop shoaling preferences for familiar males over a 12 day period, at which time they showed a clear preference for familiar over non‐familiar males.     

Social preferences in farmed silver fox females (Vulpes vulpes): Does it change with age?

Determining foxes’ social preference, and how this influences their social behaviour towards different conspecifics at different ages may give us a better understanding of how to prevent foxes from exposure of possible social stressors when housed in groups. Here, we investigated the effect of familiarity on social preferences in silver fox females and their motives for seeking social contact at two different ages. Fourteen silver fox females conducted two preference tests, first at the age of 9 weeks and the second at the age of 24 weeks, where they could choose between an empty cage, a familiar female or an unfamiliar female at their own age. The position and behaviour of the females were recorded using instantaneous sampling every tenth minute for 26 h. There was a clear preference to seek contact with a conspecific at 9 weeks of age (p < 0.01). The cubs did not differentiate between a familiar or unfamiliar stimulus animal (p > 0.05), however there was a tendency to play more in front of the unfamiliar stimulus animal (p = 0.07). No preference was seen for either the familiar, unfamiliar or empty cage stimulus when the females were 24 weeks old (p > 0.05), however they were more aggressive towards the unfamiliar stimulus animal (p < 0.01). Thus, there was no effect of familiarity in time spent with a social stimulus at either age, however these results suggest that the motives for seeking contact as cubs were non-aggressive and possibly play related, whereas the aggressive behaviour displayed by juveniles towards the unfamiliar female indicates an increased competitive motivation.     

Plasticity of olfactory orientation to foods in the snailAchatina fulica

Summary Snails were tested in an olfactometer for their orientation to food odours. Measures of odour choice, latency to make a choice and percentage of upwind orientations were obtained after experimental manipulations of dietary experience and hunger motivation. Juvenile snails, given an exclusive diet of a certain food for 12 h or less, oriented preferentially toward the odour of that food when subsequently presented with a choice between it and a novel food odour (Fig. 2). A 48 h period of exposure to a food resulted in a 21 day retention of the odour preference (Fig. 3). There was no evidence for an especially sensitive period for conditioning during the first 50 days of age (Fig. 4); however, adult snails (minimum 1 year old) required longer periods of dietary exposure to establish equivalent food odour memories (Fig. 5). Measures of latency and percentage of upwind orientations confirmed the choice data in demonstrating an effect of dietary experiences on olfactory orientation. Hunger motivation increased the selection for familiar food odours, and reduced the latency (Fig. 6 and Tables 3 and 4). Sensory adaptation appears inadequate to explain the conditioning phenomenon since formation of the preferences was contingent upon ingestion of the foods; exposure to the food odours alone was insufficient (Table 2). The data suggest that orientation preferences derive from a learned association between the odour of a food and its nutritional value.We thank Dr. Donald Kramer for helpful criticism throughout the course of this work. The research was supported financially by the National Research Council of Canada and le Ministère de l'Education du Québec.     

Estrogen treatment during development alters adult partner preference and reproductive behavior in female laboratory rats

There is broad acceptance for the idea that during development estradiol ‘organizes’ many aspects of reproductive behavior including partner preferences in the laboratory rat. With respect to partner preference, this idea is drawn from studies where estrogen action was in someway blocked, either through aromatase or estrogen receptor inhibition, during development in male rats. The lack of estrogens neonatally results in a decrease in the male rat's preference for females. In this study, the effect of early postnatal estradiol treatment on the partner preferences of female rats was examined as a further test of the hypothesis that male-typical partner preference is dependent upon early exposure to estrogens. Our principal finding was that increased postnatal estradiol exposure during development affected partner preference in the expected direction, and this effect was seen under several adult hormonal and behavioral testing conditions. Female rats that received exogenous estradiol during development spent more time with an estrous female and less time with a sexually active male than did cholesterol treated females. The estradiol treatment also disrupted normal female sexual behavior, receptivity, and proceptivity.     

Object/Context Specific Memory Deficits following Medial Frontal Cortex Damage in Mice

Recent evidence suggests that the medial prefrontal cortex (MFC) is important for processing contextual information. Here we evaluate the performance of mice with MFC damage in a discrimination task that requires an association between an object and the context in which it was experienced (the object/context mismatch task), as well as a version of the novel object preference task that does not require knowledge of contextual information to resolve. Adult C57/BL6 mice received aspiration lesions of the MFC or control surgery. Upon recovery, mice were tested in the object/context mismatch and novel object preference tasks. The object/context mismatch task involved exposing mice to two different contexts, each of which housed a unique pair of identical objects. After a brief delay, mice were re-exposed to one of the contexts, this time with one object that was congruent with that context and one that was not. Novel object preference was performed within a single context, housing an identical pair of objects. After the initial exposure and following a brief delay, mice were re-exposed to the context, this time housing a familiar and a novel object. Control mice were able to successfully resolve the object/context mismatch and novel object preference discriminations, investigating the incongruent/novel object within each task significantly greater than chance. Mice with MFC damage experienced deficits in the object/context mismatch task but not the novel object preference task. These findings add to a growing body of evidence that demonstrate a critical role for the MFC in contextual information processing.     

MECHANISMS OF AVIAN IMPRINTING: A REVIEW

Filial imprinting is the process through which early social preferences become restricted to a particular object or class of objects. Evidence is presented showing that filial preferences are formed not only as a result of learning through exposure to an object, but also under the influence of visual and auditory predispositions. The development of these predispositions is dependent upon certain non-specific experience. There is little evidence for an endogenously affected sensitive period for imprinting. It is more likely that the end of sensitivity is a result of the imprinting process itself. Similarly, it is now firmly established that filial and sexual preferences are reversible. Evidence suggests, however, that the first stimulus to which the young animal is exposed may exert a greater influence on filial preferences than subsequent stimuli. The learning process of imprinting is often regarded as being different from conventional associative learning. However, the imprinting object itself can function as a reinforcer. Recent studies have attempted to test predictions from an interpretation of filial imprinting as a form of associative learning. The first results suggest that ‘blocking’ may occur in imprinting, whilst there is no evidence for ‘overshadowing’. Social interactions with siblings and parent(-surrogates) have been shown to affect the formation of filial and sexual preferences. The influence of these interactions is particularly prominent in sexual imprinting, making earlier claims about naive species-specific biases unlikely. Although auditory stimuli play an important role in the formation of social attachments, there is little evidence for auditory imprinting per se. Auditory preferences formed as a result of mere (pre- or postnatal) exposure are relatively weak and short-lasting. Exposure to visual stimuli during auditory training significantly improves auditory learning, possibly through a process of reinforcement. It is becoming increasingly clear that filial and sexual imprinting are two different (although perhaps analogous) processes. Different mechanisms are likely to underlie the two processes, although there is evidence to suggest that the same brain region is involved in recognition of familiar stimuli in both filial and sexual imprinting. There is little evidence for a direct role of hormones in the learning process of imprinting. Androgen metabolism may be a factor constraining the development of a predisposition in the chick. Research into the neural mechanism of filial imprinting in the chick has revealed that a restricted part of the forebrain (IMHV) is likely to be a site of memory storage. Changes in synapse morphology and in the number of NMDA receptors have been found, limited to this region, and correlated with the strength of preference.     

Cross-species familiarity in shoaling fishes

Preferential association with familiar shoal mates confers a number of potentially important benefits to individuals, including improved anti-predator effects and the reduction of aggression in competitive interactions. Until now, however, familiarity has been demonstrated purely between conspecifics. Here, we present evidence that familiarity preferences can override natural preferences for conspecifics. Individual focal fishes (chub, Leuciscus cephalus) were given a choice of two stimulus shoals of the same size composed of conspecifics or of heterospecifics (minnows, Phoxinus phoxinus) in a flow tank. A series of four treatments was carried out to investigate the effects of familiarity, induced by a 15 day association between the focal fish and the stimulus fishes, on the choices made by the focal fish. Focal fishes showed a significant preference for conspecifics over heterospecifics when both stimulus shoals were composed of non-familiar individuals. Focal fishes also showed a significant preference for stimulus shoals composed of familiar fishes over stimulus shoals composed of non-familiar fishes when both shoals were conspecific and when both shoals were heterospecific. Finally, the preference of focal fishes for conspecifics disappeared when the alternative, a shoal of heterospecifics, was composed of familiar individuals. The importance of this work is discussed in the context of species interactions in free-ranging shoals.     

Predator experience overrides learned aversion to heterospecifics in stickleback species pairs

Predation risk can alter female mating decisions because the costs of mate searching and selecting attractive mates increase when predators are present. In response to predators, females have been found to plastically adjust mate preference within species, but little is known about how predators alter sexual isolation and hybridization among species. We tested the effects of predator exposure on sexual isolation between benthic and limnetic threespine sticklebacks (Gasterosteus spp.). Female discrimination against heterospecific mates was measured before and after females experienced a simulated attack by a trout predator or a control exposure to a harmless object. In the absence of predators, females showed increased aversion to heterospecifics over time. We found that predator exposure made females less discriminating and precluded this learned aversion to heterospecifics. Benthic and limnetic males differ in coloration, and predator exposure also affected sexual isolation by weakening female preferences for colourful males. Predator effects on sexual selection were also tested but predators had few effects on female choosiness among conspecific mates. Our results suggest that predation risk may disrupt the cognitive processes associated with mate choice and lead to fluctuations in the strength of sexual isolation between species.     

Mating Preferences of the Gynogenetic Amazon Molly Differ Between Populations Sympatric with Different Host Species

Gynogenetic species rely on sperm from heterospecifics for reproduction but do not receive genetic benefits from mating because none of the paternal genome is incorporated into offspring. The gynogenetic Amazon molly (Poecilia formosa) is a species of hybrid origins that are sympatric with one of the two parent species that provide sperm for reproduction, P. latipinna or P. mexicana. Amazons should not prefer to mate with one species over the other because sperm from both species will trigger embryogenesis, but mating preferences may be present in Amazons through other mechanisms. Amazons may prefer the more familiar species (males found in sympatry), or Amazons may prefer males with the greatest lateral projection area (LPA), a preference that is present in the parent species and may be retained within the Amazon hybrid genome. We tested association preferences of two populations of Amazons sympatric with either P. mexicana or P. latipinna. We first performed live trials to test whether Amazons preferred one host species over the other and found that neither population of Amazons showed a preference. We then tested whether Amazons preferred sympatric male (familiar) host or the male with the greatest lateral projection area (LPA) using four animated male models that varied in host species and manipulation of LPA. We found Amazons from a population sympatric with P. latipinna showed no variation in their association preference across the different models. In contrast, Amazons from a population sympatric with P. mexicana (naturally small LPA) spent more time associating with the male models that had smaller LPA, which is more familiar to this population of Amazons. We suggest that Amazons may have population differences in mating preferences, where Amazons sympatric with P. latipinna may not show mating preference for host species, but Amazons sympatric with P. mexicana may show preferences for more familiar‐shaped males.     

Perception of novel changes in a familiar environment by socially‐housed rhesus monkeys

Many animals appear to have a sophisticated spatial representation of their environment. The development of these representations depends on the joint abilities of discriminating novel objects and remembering their locations. Variations of a detection of novelty paradigm were used to determine the nature and limitations of these abilities in rhesus monkeys. Socially‐housed monkeys at two facilities (UMASS Primate Laboratory and the New England Regional Primate Research Center) were exposed to novelty detection tasks using a vertical object grid arranged on a mesh wall of the animals' pens. Monkeys rapidly responded with increased exploration to the replacement of one familiar object with a novel object, to the movement of a familiar object to a novel location, and to the swapping of two familiar objects. However, novelty of object was more salient than novelty of place. In these initial studies, monkeys were given continuous access to the grid, and only one or two changes occurred on a given day. In subsequent studies, the task difficulty was varied either by reducing the length of grid exposure or increasing the number of changed objects/session. Surprisingly, only a reduction in length of exposure markedly affected novelty detecting abilities. Rhesus monkeys clearly possessed the dual novelty detecting abilities. These skills were negatively affected only when monkeys' access to the grid was limited. The procedure employed here provided a convenient way to assess complex cognitive abilities in a group setting. It also relied on rhesus monkeys' inherent attraction to novelty and required only their species‐typical behavior for assessment. Am. J. Primatol. 47:117–131, 1999. © 1999 Wiley‐Liss, Inc.     

Transgenerational inheritance of learned preferences for novel host plant odors in Bicyclus anynana butterflies

Many phytophagous insects have strong preferences for their host plants, which they recognize via odors, making it unclear how novel host preferences develop in the course of insect diversification. Insects may learn to prefer new host plants via exposure to their odors and pass this learned preference to their offspring. We tested this hypothesis by examining larval odor preferences before and after feeding them with leaves coated with control and novel odors and by examining odor preferences again in their offspring. Larvae of the parental generation developed a preference for two of these odors over their development. These odor preferences were also transmitted to the next generation. Offspring of butterflies fed on these new odors chose these odors more often than offspring of butterflies fed on control leaves. In addition, offspring of butterflies fed on banana odors had a significant naïve preference for the banana odors in contrast to the naïve preference for control leaves shown by individuals of the parental generation. Thus, butterflies can learn to prefer novel host plant odors via exposure to them during larval development and transmit these learned preferences to their offspring. This ability potentially facilitates shifts in host plant use over the course of insect diversification.