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Brennan, P. A. (2004). The nose knows who's who: chemosensory individuality and mate recognition in mice. Horm Behav, 46(3), 231–240.
Abstract: Individual recognition is an important component of behaviors, such as mate choice and maternal bonding that are vital for reproductive success. This article highlights recent developments in our understanding of the chemosensory cues and the neural pathways involved in individuality discrimination in rodents. There appear to be several types of chemosensory signal of individuality that are influenced by the highly polymorphic families of major histocompatibility complex (MHC) proteins or major urinary proteins (MUPs). Both have the capability of binding small molecules and may influence the individual profile of these chemosignals in biological fluids such as urine, skin secretions, or saliva. Moreover, these proteins, or peptides associated with them, can be taken up into the vomeronasal organ (VNO) where they can potentially interact directly with the vomeronasal receptors. This is particularly interesting given the expression of major histocompatibility complex Ib proteins by the V2R class of vomeronasal receptor and the highly selective responses of accessory olfactory bulb (AOB) mitral cells to strain identity. These findings are consistent with the role of the vomeronasal system in mediating individual discrimination that allows mate recognition in the context of the pregnancy block effect. This is hypothesized to involve a selective increase in the inhibitory control of mitral cells in the accessory olfactory bulb at the first level of processing of the vomeronasal stimulus.
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Brennan, P. A., & Kendrick, K. M. (2006). Mammalian social odours: attraction and individual recognition. Phil. Trans. Biol. Sci., 361(1476), 2061–2078.
Abstract: Mammalian social systems rely on signals passed between individuals conveying information including sex, reproductive status, individual identity, ownership, competitive ability and health status. Many of these signals take the form of complex mixtures of molecules sensed by chemosensory systems and have important influences on a variety of behaviours that are vital for reproductive success, such as parent-offspring attachment, mate choice and territorial marking. This article aims to review the nature of these chemosensory cues and the neural pathways mediating their physiological and behavioural effects. Despite the complexities of mammalian societies, there are instances where single molecules can act as classical pheromones attracting interest and approach behaviour. Chemosignals with relatively high volatility can be used to signal at a distance and are sensed by the main olfactory system. Most mammals also possess a vomeronasal system, which is specialized to detect relatively non-volatile chemosensory cues following direct contact. Single attractant molecules are sensed by highly specific receptors using a labelled line pathway. These act alongside more complex mixtures of signals that are required to signal individual identity. There are multiple sources of such individuality chemosignals, based on the highly polymorphic genes of the major histocompatibility complex (MHC) or lipocalins such as the mouse major urinary proteins. The individual profile of volatile components that make up an individual odour signature can be sensed by the main olfactory system, as the pattern of activity across an array of broadly tuned receptor types. In addition, the vomeronasal system can respond highly selectively to non-volatile peptide ligands associated with the MHC, acting at the V2r class of vomeronasal receptor.The ability to recognize individuals or their genetic relatedness plays an important role in mammalian social behaviour. Thus robust systems for olfactory learning and recognition of chemosensory individuality have evolved, often associated with major life events, such as mating, parturition or neonatal development. These forms of learning share common features, such as increased noradrenaline evoked by somatosensory stimulation, which results in neural changes at the level of the olfactory bulb. In the main olfactory bulb, these changes are likely to refine the pattern of activity in response to the learned odour, enhancing its discrimination from those of similar odours. In the accessory olfactory bulb, memory formation is hypothesized to involve a selective inhibition, which disrupts the transmission of the learned chemosignal from the mating male. Information from the main olfactory and vomeronasal systems is integrated at the level of the corticomedial amygdala, which forms the most important pathway by which social odours mediate their behavioural and physiological effects. Recent evidence suggests that this region may also play an important role in the learning and recognition of social chemosignals.
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Brodbeck, D. R. (1997). Picture fragment completion: priming in the pigeon. J Exp Psychol Anim Behav Process, 23(4), 461–468.
Abstract: It has been suggested that the system behind implicit memory in humans is evolutionarily old and that animals should readily show priming. In Experiment 1, a picture fragment completion test was used to test priming in pigeons. After pecking a warning stimulus, pigeons were shown 2 partially obscured pictures from different categories and were always reinforced for choosing a picture from one of the categories. On control trials, the warning stimulus was a picture of some object (not from the S+ or S- category), on study trials the warning stimulus was a picture to be categorized on the next trial, and on test trials the warning stimulus was a randomly chosen picture and the S+ picture was the warning stimulus seen on the previous trial. Categorization was better on study and test trials than on control trials. Experiment 2 ruled out the possibility that the priming effect was caused by the pigeons' responding to familiarity by using warning stimuli from both S+ and S- categories. Experiment 3 investigated the time course of the priming effect.
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Chiandetti, C., Regolin, L., Sovrano, V. A., & Vallortigara, G. (2007). Spatial reorientation: the effects of space size on the encoding of landmark and geometry information. Anim. Cogn., 10(2), 159–168.
Abstract: The effects of the size of the environment on animals' spatial reorientation was investigated. Domestic chicks were trained to find food in a corner of either a small or a large rectangular enclosure. A distinctive panel was located at each of the four corners of the enclosures. After removal of the panels, chicks tested in the small enclosure showed better retention of geometrical information than chicks tested in the large enclosure. In contrast, after changing the enclosure from a rectangular-shaped to a square-shaped one, chicks tested in the large enclosure showed better retention of landmark (panels) information than chicks tested in the small enclosure. No differences in the encoding of the overall arrangement of landmarks were apparent when chicks were tested for generalisation in an enclosure differing from that of training in size together with a transformation (affine transformation) that altered the geometric relations between the target and the shape of the environment. These findings suggest that primacy of geometric or landmark information in reorientation tasks depends on the size of the experimental space, likely reflecting a preferential use of the most reliable source of information available during visual exploration of the environment.
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Christensen, J. W., Zharkikh, T., & Chovaux, E. (2011). Object recognition and generalisation during habituation in horses. Appl. Anim. Behav. Sci., 129(2-4), 83–91.
Abstract: The ability of horses to habituate to frightening stimuli greatly increases safety in the horse-human relationship. A recent experiment suggested, however, that habituation to frightening visual stimuli is relatively stimulus-specific in horses and that shape and colour are important factors for object generalisation (Christensen et al., 2008). In a series of experiments, we aimed to further explore the ability of horses (n = 30, 1 and 2-year-old mares) to recognise and generalise between objects during habituation. TEST horses (n = 15) were habituated to a complex object, composed of five simple objects of varying shape and colour, whereas CONTROL horses (n = 15) were habituated to the test arena, but not to the complex object. In the first experiment, we investigated whether TEST horses subsequently reacted less to i) simple objects that were previously part of the complex object (i.e. testing for object recognition) and ii) a novel object (new shape and colour, i.e. testing for object generalisation), compared to CONTROLS. In the second experiment we investigated whether TEST horses reacted to a change in object order and object location. Behavioural reactions to the object, latency to eat, total eating time and heart rate were recorded. Compared to CONTROLS, TEST horses reacted significantly less towards objects, which were previously part of the complex object (e.g. mean heart rate; P = 0.006), indicating object recognition. In contrast to our expectations, TEST horses also reacted significantly less towards the novel object (e.g. mean heart rate; P = 0.018), suggesting that they were capable of object generalisation. We also found that TEST horses showed an increase in exploratory behaviour when objects within the complex object changed order and location (both P < 0.001), whereas there was no increase in heart rate, indicating that the horses were not frightened by the changes. The results demonstrate that it is possible to increase object generalisation in horses by habituating them to a range of colours and shapes simultaneously. This knowledge greatly affects the way in which horses may be trained to react calmly towards frightening objects.
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Clara, E., Regolin, L., Vallortigara, G., & Rogers, L. (2007). Perception of the stereokinetic illusion by the common marmoset (Callithrix jacchus). Anim. Cogn., 10(2), 135–140.
Abstract: Stereokinetic illusions have never been investigated in non-human primates, nor in other mammalian species. These illusions consist in the perception of a 3D solid object when certain 2D stimuli are rotated slowly in the plane perpendicular to the line of sight. The ability to perceive the stereokinetic illusion was investigated in the common marmoset (Callithrix jacchus). Four adult marmosets were trained to discriminate between a solid cylinder and a solid cone for food reward. Once learning criterion was reached, the marmosets were tested in sets of eight probe trials in which the two solid objects used at training were replaced by two rotating 2D stimuli. Only one of these stimuli produced, at least to the human observer, the stereokinetic illusion corresponding to the solid object previously reinforced. At test, the general behaviour and the total time spent by the marmosets observing each stimulus were recorded. The subjects stayed longer near the stimulus producing the stereokinetic illusion corresponding to the solid object reinforced at training than they did near the illusion corresponding to the previously non-rewarded stimulus. Hence, the common marmosets behaved as if they could perceive stereokinetic illusions.
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Clement, T. S., & Zentall, T. R. (2000). Development of a single-code/default coding strategy in pigeons. Psychol Sci, 11(3), 261–264.
Abstract: We tested the hypothesis that pigeons could use a cognitively efficient coding strategy by training them on a conditional discrimination (delayed symbolic matching) in which one alternative was correct following the presentation of one sample (one-to-one), whereas the other alternative was correct following the presentation of any one of four other samples (many-to-one). When retention intervals of different durations were inserted between the offset of the sample and the onset of the choice stimuli, divergent retention functions were found. With increasing retention interval, matching accuracy on trials involving any of the many-to-one samples was increasingly better than matching accuracy on trials involving the one-to-one sample. Furthermore, following this test, pigeons treated a novel sample as if it had been one of the many-to-one samples. The data suggest that rather than learning each of the five sample-comparison associations independently, the pigeons developed a cognitively efficient single-code/default coding strategy.
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Crowley, P. H., Provencher, L., Sloane, S., Dugatkin, L. A., Spohn, B., Rogers, L., et al. (1996). Evolving cooperation: the role of individual recognition. Biosystems, 37(1-2), 49–66.
Abstract: To evaluate the role of individual recognition in the evolution of cooperation, we formulated and analyzed a genetic algorithm model (EvCo) for playing the Iterated Prisoner's Dilemma (IPD) game. Strategies compete against each other during each generation, and successful strategies contribute more of their attributes to the next generation. Each strategy is encoded on a `chromosome' that plays the IPD, responding to the sequences of most recent responses by the interacting individuals (chromosomes). The analysis reported in this paper considered different memory capabilities (one to five previous interactions), pairing continuities (pairs of individuals remain together for about one, two, five, or 1000 consecutive interactions), and types of individual recognition (recognition capability was maximal, nil, or allowed to evolve between these limits). Analysis of the results focused on the frequency of mutual cooperation in pairwise interactions (a good indicator of overall success in the IPD) and on the extent to which previous responses by the focal individual and its partner were associated with the partner's identity (individual recognition). Results indicated that a fixed, substantial amount of individual recognition could maintain high levels of mutual cooperation even at low pairing continuities, and a significant but limited capability for individual recognition evolved under selection. Recognition generally increased mutual cooperation more when the recent responses of individuals other than the current partner were ignored. Titrating recognition memory under selection using a fitness cost suggested that memory of the partner's previous responses was more valuable than memory of the focal's previous responses. The dynamics produced to date by EvCo are a step toward understanding the evolution of social networks, for which additional benefits associated with group interactions must be incorporated.
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De Boyer Des Roches, A., Richard-Yris, M. - A., Henry, S., Ezzaouia, M., & Hausberger, M. (2008). Laterality and emotions: visual laterality in the domestic horse (Equus caballus) differs with objects' emotional value. Physiol. Behav., 94(3), 487–490.
Abstract: Lateralization of emotions has received great attention in the last decades, both in humans and animals, but little interest has been given to side bias in perceptual processing. Here, we investigated the influence of the emotional valence of stimuli on visual and olfactory explorations by horses, a large mammalian species with two large monocular visual fields and almost complete decussation of optic fibres. We confronted 38 Arab mares to three objects with either a positive, negative or neutral emotional valence (novel object). The results revealed a gradient of exploration of the 3 objects according to their emotional value and a clear asymmetry in visual exploration. When exploring the novel object, mares used preferentially their right eyes, while they showed a slight tendency to use their left eyes for the negative object. No asymmetry was evidenced for the object with the positive valence. A trend for an asymmetry in olfactory investigation was also observed. Our data confirm the role of the left hemisphere in assessing novelty in horses like in many vertebrate species and the possible role of the right hemisphere in processing negative emotional responses. Our findings also suggest the importance of both hemispheres in the processing positive emotions. This study is, to our knowledge, the first to demonstrate clearly that the emotional valence of a stimulus induces a specific visual lateralization pattern.
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de Waal, F. B. M., Dindo, M., Freeman, C. A., & Hall, M. J. (2005). The monkey in the mirror: hardly a stranger. Proc. Natl. Acad. Sci. U.S.A., 102(32), 11140–11147.
Abstract: It is widely assumed that monkeys see a stranger in the mirror, whereas apes and humans recognize themselves. In this study, we question the former assumption by using a detailed comparison of how monkeys respond to mirrors versus live individuals. Eight adult female and six adult male brown capuchin monkeys (Cebus apella) were exposed twice to three conditions: (i) a familiar same-sex partner, (ii) an unfamiliar same-sex partner, and (iii) a mirror. Females showed more eye contact and friendly behavior and fewer signs of anxiety in front of a mirror than they did when exposed to an unfamiliar partner. Males showed greater ambiguity, but they too reacted differently to mirrors and strangers. Discrimination between conditions was immediate, and blind coders were able to tell the difference between monkeys under the three conditions. Capuchins thus seem to recognize their reflection in the mirror as special, and they may not confuse it with an actual conspecific. Possibly, they reach a level of self-other distinction intermediate between seeing their mirror image as other and recognizing it as self.
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