Images Of Conspecifics Research Articles

How do goats "read" 2D-images of familiar and unfamiliar conspecifics?

To study individual recognition in animals, discrimination tasks are often conducted by presenting 2D images of real conspecifics. However, animals may discriminate the images merely as visual stimulus combinations without establishing referential relationships to the individuals depicted. In the current study, we investigated whether goats are able to discriminate photos of familiar and unfamiliar conspecifics, whether they not only process the photos as visual stimuli, but also understand them as virtual copies of real conspecifics and whether they grasp the concept of familiarity. Using a computer-controlled learning device, in three tests, goats of two experimental groups (A and B) had to discriminate portrait (Te1), profile (Te2) or headless body photos (Te3) of conspecifics. Tests were presented as 4-choice tasks, with one photo from Group A (rewarded) plus three photos from Group B (distractors). That is, the rewarded photo was familiar to Group A, but unfamiliar to Group B. Finally, in a reversal test (Te4) we reversed this principle. The goats learned the discriminations in Te1 to Te3 within two (Te1 and Te2) and three training days (Te3), respectively, and they needed between 91 [CL (66, 126)] and 174 [CL (126, 241)] trials to reach the learning criterion, with no statistically significant differences between the groups. In Te4, in contrast, the animals took 403 [Group A; CL (291, 557)] and 385 [Group B; CL (286, 519)] trials, respectively, to learn the task. The lack of spontaneous preferences for the photo of the familiar conspecific in the pretests of Te1 to Te3 in Group A, as well as the lack of differences in the number of trials to learn the discriminations between both groups, do not at first glance suggest that the goats established a correspondence between real conspecifics and their 2D representations. However, the higher number of trials in Te4 suggests that both groups formed the learning rule of choosing either the known (Group A) or the unknown goat (Group B) over the course of Te1 to Te3 and then failed after the rule was reversed, providing evidence that goats can associate 2D photos of conspecifics with real animals.

Friend or foe? Using eye-tracking technology to investigate the visual discrimination ability of giant pandas.

The role that visual discriminative ability plays among giant pandas in social communication and individual discrimination has received less attention than olfactory and auditory modalities. Here, we used an eye-tracker technology to investigate pupil fixation patterns for 8 captive male giant pandas Ailuropoda melanoleuca. We paired images (N = 26) of conspecifics against: 1) sympatric predators (gray wolves and tigers), and non-threatening sympatric species (golden pheasant, golden snub-nosed monkey, takin, and red panda), 2) conspecifics with atypical fur coloration (albino and brown), and 3) zookeepers/non-zookeepers wearing either work uniform or plain clothing. For each session, we tracked the panda's pupil movements and measured pupil first fixation point (FFP), fixation latency, total fixation count (TFC), and duration (TFD) of attention to each image. Overall, pandas exhibited similar attention (FFPs and TFCs) to images of predators and non-threatening sympatric species. Images of golden pheasant, snub-nosed monkey, and tiger received less attention (TFD) than images of conspecifics, whereas images of takin and red panda received more attention, suggesting a greater alertness to habitat or food competitors than to potential predators. Pandas' TFCs were greater for images of black-white conspecifics than for albino or brown phenotypes, implying that familiar color elicited more interest. Pandas reacted differently to images of men versus women. For images of women only, pandas gave more attention (TFC) to familiar combinations (uniformed zookeepers and plain-clothed non-zookeepers), consistent with the familiarity hypothesis. That pandas can use visual perception to discriminate intra-specifically and inter-specifically, including details of human appearance, has applications for panda conservation and captive husbandry.

Attention to Stimuli of Learned versus Innate Biological Value Relies on Separate Neural Systems.

The neural bases of attention, a set of neural processes that promote behavioral selection, is a subject of intense investigation. In humans, rewarded cues influence attention, even when those cues are irrelevant to the current task. Because the amygdala plays a role in reward processing, and the activity of amygdala neurons has been linked to spatial attention, we reasoned that the amygdala may be essential for attending to rewarded images. To test this possibility, we used an attentional capture task, which provides a quantitative measure of attentional bias. Specifically, we compared reaction times (RTs) of adult male rhesus monkeys with bilateral amygdala lesions and unoperated controls as they made a saccade away from a high- or low-value rewarded image to a peripheral target. We predicted that: (1) RTs will be longer for high- compared with low-value images, revealing attentional capture by rewarded stimuli; and (2) relative to controls, monkeys with amygdala lesions would exhibit shorter RT for high-value images. For comparison, we assessed the same groups of monkeys for attentional capture by images of predators and conspecifics, categories thought to have innate biological value. In performing the attentional capture task, all monkeys were slowed more by high-value relative to low-value rewarded images. Contrary to our prediction, amygdala lesions failed to disrupt this effect. When presented with images of predators and conspecifics, however, monkeys with amygdala lesions showed significantly diminished attentional capture relative to controls. Thus, separate neural pathways are responsible for allocating attention to stimuli with learned versus innate value.SIGNIFICANCE STATEMENT Valuable objects attract attention. The amygdala is known to contribute to reward processing and the encoding of object reward value. We therefore examined whether the amygdala is necessary for allocating attention to rewarded objects. For comparison, we assessed the amygdala's contribution to attending to objects with innate biological value: predators and conspecifics. We found that the macaque amygdala is necessary for directing attention to images with innate biological value, but not for directing attention to recently learned reward-predictive images. These findings indicate that the amygdala makes selective contributions to attending to valuable objects. The data are relevant to mental health disorders, such as social anxiety disorders and small animal phobias, that arise from biased attention to select categories of objects.

Bonobos and chimpanzees preferentially attend to familiar members of the dominant sex

Social animals must carefully track consequential events and opportunities for social learning. However, the competing demands of the social world produce trade-offs in social attention, defined as directed visual attention towards conspecifics. A key question is how socioecology shapes these biases in social attention over evolution and development. Chimpanzees, Pan troglodytes , and bonobos, Pan paniscus , provide ideal models for addressing this question because they have large communities with fission–fusion grouping, divergent sex-based dominance hierarchies and occasional intergroup encounters. Using noninvasive eye-tracking measures, we recorded captive apes’ attention to side-by-side images of familiar and unfamiliar conspecifics of the same sex. We tested four competing hypotheses about the influence of taxonomically widespread socioecological pressures on social attention, including intergroup conflict, dominance, dispersal and mating competition. Both species preferentially attended to familiar over unfamiliar conspecifics when viewing the sex that typically occupies the highest ranks in the group: females for bonobos, and males for chimpanzees. However, they did not demonstrate attentional biases between familiar and unfamiliar members of the subordinate sex. Findings were consistent across species despite differences in which sex tends to be more dominant. These results suggest that sex-based dominance patterns guide social attention across Pan . Our findings reveal how socioecological pressures shape social attention in apes and likely contribute to the evolution of social cognition across primates. • Bonobos and chimpanzees discriminate faces of familiar and unfamiliar conspecifics. • Great apes devote greater social attention to familiar members of the dominant sex. • Species differences in male vs female dominance shape patterns of social attention. • Both selective pressures and socialization likely drive patterns of social attention.

Interspecific two-dimensional visual discrimination of faces in horses (Equus caballus).

In social animals, recognizing conspecifics and distinguishing them from other animal species is certainly important. We hypothesize, as demonstrated in other species of ungulates, that horses are able to discriminate between the faces of conspecifics and the faces of other domestic species (cattle, sheep, donkeys and pigs). Our hypothesis was tested by studying inter-and intra-specific visual discrimination abilities in horses through a two-way instrumental conditioning task (discrimination and reversal learning), using two-dimensional images of faces as discriminative stimuli and food as a positive reward. Our results indicate that 8 out of 10 horses were able to distinguish between two-dimensional images of the faces of horses and images showing the faces of other species. A similar performance was obtained in the reversal task. The horses' ability to learn by discrimination is therefore comparable to other ungulates. Horses also showed the ability to learn a reversal task. However, these results were obtained regardless of the images the tested horses were exposed to. We therefore conclude that horses can discriminate between two dimensional images of conspecifics and two dimensional images of different species, however in our study, they were not able to make further subcategories within each of the two categories. Despite the fact that two dimensional images of animals could be treated differently from two dimensional images of non-social stimuli, our results beg the question as to whether a two-dimensional image can replace the real animal in cognitive tests.

Rainbow trout discriminate 2-D photographs of conspecifics from distracting stimuli using an innovative operant conditioning device.

Cognitive abilities were studied in rainbow trout, the first continental fish production in Europe. Increasing public concern for the welfare of farmed-fish species highlighted the need for better knowledge of the cognitive status of fish. We trained and tested 15 rainbow trout with an operant conditioning device composed of self-feeders positioned in front of visual stimuli displayed on a screen. The device was coupled with a two-alternative forced-choice (2-AFC) paradigm to test whether rainbow trout can discriminate 2-D photographs of conspecifics (S+) from different visual stimuli (S-). The S- were applied in four stages, the last three stages representing increasing discrimination difficulty: (1) blue shapes; (2) black shape (star); (3) photograph of an object (among a pool of 60); (4) photograph of another fish species (among a pool of 60). Nine fish (out of 15) correctly managed to activate the conditioning device after 30-150 trials. The rainbow trout were able to discriminate images of conspecifics from an abstract shape (five individuals out of five) or objects (four out of five) but not from other fish species. Their ability to learn the category "fish shape" rather than distinguishing between conspecifics and heterospecifics is discussed. The successful visual discrimination task using this complex operant conditioning device is particularly remarkable and novel for this farmed-fish species, and could be exploited to develop cognitive enrichments in future farming systems. This device can also be added to the existing repertoire of testing devices suitable for investigating cognitive abilities in fish.

Attention to social stimuli is modulated by sex and exposure time in tufted capuchin monkeys

The dot probe task is an experimental procedure commonly used to study how animals (including humans) pay attention to different stimuli. In this study, we evaluated how different durations of image exposure modulate the response to this task and how male and female tufted capuchin monkeys (Sapajus spp.) respond to a dot probe presented immediately after different social stimuli. Subjects were shown pairs of images of unfamiliar conspecifics: a male versus a female or two individuals grooming versus two individuals not engaged in grooming (nongrooming). With shorter image exposures (250 ms) both sexes showed shorter response times to the dot probe after presentation of (i.e. biased their attention towards) images of unfamiliar males compared to females, and did not show any bias towards images of grooming compared to nongrooming. With longer image exposures (1000 ms) females biased their attention towards images of unfamiliar females, while males did not show any difference; in contrast, males biased their attention towards images of grooming compared to nongrooming, while females did not show any difference. We interpret these results as showing that responses to the dot probe task with different image exposures reflect different attentional phenomena, and that the two sexes differ in how social stimuli affect their attention.

Chimpanzees, but not bonobos, attend more to infant than adult conspecifics

Primate infants have several physical features that distinguish them from adults in appearance. One such feature is the well-known ‘baby schema,’ in which the infant has a relatively large head and eyes, and a small nose and mouth. Humans typically prefer infants of both conspecifics and heterospecifics with a strong baby schema. In nonhuman primates, infants of some (e.g. chimpanzees, Pan troglodytes) but not all species (e.g. bonobos, Pan paniscus) have species-specific conspicuous skin and fur coloration, in addition to species-common infantile features. This study examined whether closely related chimpanzees and bonobos have a preference for infants, and, if so, whether they are attracted to species-common features (e.g. the relatively large head and eyes) or species-specific features (e.g. conspicuous coloration). We used eye tracking to measure eye movements while participants viewed naturalistic images of a mother–infant pair. We adopted a cross-species design, so that both species viewed images of chimpanzees, bonobos and an outgroup primate species. We found that chimpanzees viewed the faces of infants for longer than those of adults when presented with conspecific images, but not when presented with heterospecific images. Chimpanzees also did not show any preference when facial coloration was matched between conspecific infants and adults in a follow-up experiment. Chimpanzees thus seem to respond particularly to the special infantile coloration of conspecifics. Bonobos clearly differed from chimpanzees in that they did not view conspecific infants for longer than adults and viewed heterospecific adults for longer than infants. These observed species differences may be related to their species-typical social and rearing styles. In conclusion, the preference for infants is species-specific in bonobos and chimpanzees, with a general lack of preference for the species-common baby schema.

A competitive drive? Same-sex attentional preferences in capuchins.

In primates, faces provide information about several characteristics of social significance, including age, physical health, and biological sex. However, despite a growing literature on face processing and visual attention in a number of primate species, preferences for same- or opposite-sex faces have not yet been examined. In the current study, we explore the role of conspecific sex on visual attention in two groups of capuchin monkeys. Subjects were shown a series of image pairs on a Tobii Pro TX300 eye tracker, each depicting an unfamiliar male and an unfamiliar female face. Given the behavioral evidence of mate choice in both sexes, we hypothesized that capuchins would preferentially attend to images of unfamiliar conspecifics of the opposite sex. Our alternative hypothesis was that capuchins would preferentially attend to same-sex individuals to assess potential competitors. Our results provide support for our alternative hypothesis. When comparing attention to each stimuli type across sexes, females spent significantly larger percentages of time than males looking at female photos, whereas males spent significantly larger percentages of time than females looking at male photos. Within each sex, females looked for significantly larger percentages of time to female versus male images. Males also looked for larger percentages of time to same-sex images, though not significantly. To our knowledge, these data are the first to demonstrate significant sex-biased attentional preferences in adult primates of any species, and suggest that, for capuchins, potential competitors garner more attention than potential mates. In addition, our findings have implications for studies of visual attention and face processing across the primate order, and suggest that researchers need to control for these demographic factors in their experimental designs.

The Importance of Holding Water: Salinity and Chemosensory Cues Affect Zebrafish Behavior.

The zebrafish is becoming a popular model organism for studying numerous biological phenomena. Among these are brain function and behavior, including social behavior. Although usually neglected, few studies have already demonstrated that even trivial factors, such as features of the holding water may alter zebrafish behavior. In this study, we employed a 2 × 2 between-subject experimental design, exposing zebrafish to water of either high or low salinity and with chemosensory/olfactory cues of conspecifics either present or absent (while maintaining pH, temperature, nitrate, nitrite, and ammonia levels constant). We presented moving images of conspecifics to experimental zebrafish and analyzed their behavioral responses using video tracking. We found significant interaction between salinity and olfactory cues. For example, zebrafish exposed to their home tank water (high salinity with chemosensory/olfactory cues present) stayed significantly closer to the bottom of their tank compared with fish exposed to the other water conditions, and fish exposed to water with chemosensory/olfactory cues significantly reduced their turns compared with fish exposed to water without chemosensory/olfactory cues. These differences signify the impact environmental factors, for example, fluctuations in salinity level and presence or absence of chemosensory/olfactory cues, may have on zebrafish behavior. We conclude that maintaining stable environmental conditions and specifying and reporting them precisely are important for reducing error variation and for making results across independent studies more comparable.

Good night, sleep tight: The effects of sleep deprivation on spatial associative learning in zebrafish

Learning and memory are vital to an animal's survival, and numerous factors can disrupt cognitive performance. Sleep is an evolutionarily conserved physiological process known to be important for the consolidation of learning and memory. The zebrafish has emerged as a powerful model organism sharing organizational and functional characteristics with other vertebrates, providing great translational relevance. In our study, we used a simple spatial associative learning task to quantify the effects of sleep deprivation (partial vs. total) on learning performance in zebrafish, using an animated conspecific shoal image as a reward. Control animals maintained on a regular light:dark cycle were able to acquire the association between the unconditioned and conditioned stimulus, reinforcing zebrafish as a valid and reliable model for appetitive conditioning tasks. Notably, sleep deprivation did not alter the perception of and response to the conspecific image. In contrast, although partial sleep deprivation did not impair cognitive performance, total sleep deprivation significantly impaired performance on the associative learning task. Our results suggest that sleep is important for learning and memory, and that the effects of sleep deprivation on these processes can be investigated in zebrafish.

The use of preferred social stimuli as rewards for rhesus macaques in behavioural neuroscience.

Macaques are often motivated to perform in neuroscientific experiments by implementing fluid restriction protocols. Daily access to water is controlled and the monkeys are rewarded with droplets of fluid for performing correct trials in the laboratory. Although these protocols are widely used and highly effective, it is important from a 3Rs perspective to investigate refinements that may help to lessen the severity of the fluid restriction applied. We assessed the use of social stimuli (images of conspecifics) as rewards for four rhesus macaques performing simple cognitive tasks. We found that individual preferences for images of male faces, female perinea and control stimuli could be identified in each monkey. However, using preferred images did not translate into effective motivators on a trial-by-trial basis: animals preferred fluid rewards, even when fluid restriction was relaxed. There was no difference in the monkeys’ performance of a task when using greyscale versus colour images. Based on our findings, we cannot recommend the use of social stimuli, in this form, as a refinement to current fluid restriction protocols. We discuss the potential alternatives and possibilities for future research.

Visual response properties of neurons in four areas of the avian pallium.

In the present study we investigate the visual responsiveness of neurons in the entopallium, arcopallium, nidopallium, and hippocampus of pigeons. Pigeons were presented with 12 different stimuli, including three stimuli of a pigeon (a portrait of a pigeon's face, a profile view of a pigeon's face, and a picture of a whole pigeon). A total of 53 cells were recorded from the entopallium, 65 from the arcopallium, 32 from the nidopallium, and 67 from the hippocampus. Although a number of neurons were selective for certain colours and shapes, no neurons were solely selective for the three pigeon stimuli. This finding contrasts with previous studies across a range of mammals demonstrating selective firing to images of conspecifics. Rather than reflecting an absence of these cells in pigeons, we argue our findings may reflect the difficulty pigeons have in understanding the correspondence between 2D representations of 3D stimuli.

Impairment of social behaviour persists two years after embryonic alcohol exposure in zebrafish: A model of fetal alcohol spectrum disorders

Zebrafish naturally form social groups called shoals. Previously, we have shown that submerging zebrafish eggs into low concentrations of alcohol (0.00, 0.25, 0.50, 0.75 and 1.00 vol/vol% external bath concentration) during development (24h post-fertilization) for two hours resulted in impaired shoaling response in seven month old young adult zebrafish. Here we investigate whether this embryonic alcohol exposure induced behavioural deficit persists to older age. Zebrafish embryos were exposed either to fresh system water (control) or to 1% alcohol for two hours, 24h after fertilization, and were raised in a high-density tank system. Social behaviour was tested by presenting the experimental fish with a computer animated group of zebrafish images, while automated tracking software measured their behaviour. Control fish were found to respond strongly to animated conspecific images by reducing their distanceand remaining close to the images during image presentation, embryonic alcohol treated fish did not. Our results suggest that the impaired shoaling response of the alcohol exposed fish was not due to altered motor function or visual perception, but likely to a central nervous system alteration affecting social behaviour itself. We found the effects of embryonic alcohol exposure on social behaviour not to diminish with age, a result that demonstrates the deleterious and potentially life-long consequences of exposure to even small amount of alcohol during embryonic development in vertebrates.

The effect of the number and size of animated conspecific images on shoaling responses of zebrafish

The zebrafish is increasingly utilized in biomedical and psychopharmacological research aimed at modeling human brain disorders. Abnormal social behavior represents the core symptom of several neuropsychiatric and neurodevelopmental disorders. The zebrafish is a highly social species and has been proposed for modeling such disorders. Behavioral paradigms that can induce zebrafish social behavior are of importance. Here, we utilize a paradigm in which zebrafish are presented with computer animated images of conspecifics. We systematically varied the size of these images relative to the body size of the experimental fish and also investigated the potential effect of presenting different number of images in an attempt to optimize the paradigm. We report that images similar in size to the experimental fish induced a strong shoaling response (reduction of distance to the image presentation screen) both when the body size of the experimental fish was varied with the image size being held constant and when the image size was varied with the body size of the experimental fish being held constant. We also report that within the number range studied (from 1 to 8 conspecific stimulus fish), presentation of all animated shoals, but the image of a single conspecific stimulus fish, led to significant reduction of distance to the presentation screen. We conclude that the shoal image presentation paradigm induces robust social responses that are quantifiable in an automated manner, making the paradigm useful for screening of drugs and/or mutations.

Toward a better understanding of social learning, social deciding, and other-regarding preferences.

Toward a better understanding of social learning, social deciding, and other-regarding preferences.

Towards the characterization of short-term memory of zebrafish: effect of fixed versus random reward location.

The zebrafish has been proposed as an efficient tool for the analysis of behavioral and neurobiological mechanisms of learning and memory. However, compared to traditional laboratory rodents, it is a relatively newcomer. In fact, only limited information on its mnemonic and cognitive abilities has been obtained, and only a small number of learning and memory paradigms have been available for its testing. Previously, we have shown that zebrafish are capable of learning the systematic alternating sequence of reward location in a shuttle box task in which we evaluated behavioral responses manually. Here, we employ a computerized, automated version of this task. We study whether zebrafish can remember the prior location of a reward (the sight of conspecifics) when the location is fixed (constant), or when the sequence of the location of presentation randomly changes between the left and the right side of the experimental tank. We also analyze performance features including the swim speed of experimental fish as well as the temporal changes of the position of fish when the reward (stimulus) is not presented. Our results show that under both the fixed and randomly changing reward location conditions zebrafish exhibit a significant preference for the prior location of reward, albeit the preference is stronger under the fixed location condition. We conclude that adult zebrafish have short-term associative memory that can be induced and quantified in an automated manner.

Video demonstrations seed alternative problem-solving techniques in wild common marmosets.

Studies of social learning and tradition formation under field conditions have recently gained momentum, but suffer from the limited control of socio-ecological factors thought to be responsible for transmission patterns. The use of artificial visual stimuli is a potentially powerful tool to overcome some of these problems. Here, in a field experiment, we used video images of unfamiliar conspecifics performing virtual demonstrations of foraging techniques. We tested 12 family groups of wild common marmosets. Six groups received video demonstrations (footage of conspecifics either pulling a drawer open or pushing a lid upwards, in an 'artificial fruit'); the other six groups served as controls (exposed to a static image of a conspecific next to the fruit). Subjects in video groups were more manipulative and successful in opening the fruit than controls; they were also more likely to use the technique they had witnessed and thus could serve as live models for other family members. To our knowledge, this is the first study that used video demonstrations in the wild and demonstrated the potent force of social learning, even from unfamiliar conspecifics, under field conditions.

Short-term memory in zebrafish (Danio rerio)

Learning and memory represent perhaps the most complex behavioral phenomena. Although their underlying mechanisms have been extensively analyzed, only a fraction of the potential molecular components have been identified. The zebrafish has been proposed as a screening tool with which mechanisms of complex brain functions may be systematically uncovered. However, as a relative newcomer in behavioral neuroscience, the zebrafish has not been well characterized for its cognitive and mnemonic features, thus learning and/or memory screens with adults have not been feasible. Here we study short-term memory of adult zebrafish. We show animated images of conspecifics (the stimulus) to the experimental subject during 1min intervals on ten occasions separated by different (2, 4, 8 or 16min long) inter-stimulus intervals (ISI), a between subject experimental design. We quantify the distance of the subject from the image presentation screen during each stimulus presentation interval, during each of the 1-min post-stimulus intervals immediately following the stimulus presentations and during each of the 1-min intervals furthest away from the last stimulus presentation interval and just before the next interval (pre-stimulus interval), respectively. Our results demonstrate significant retention of short-term memory even in the longest ISI group but suggest no acquisition of reference memory. Because in the employed paradigm both stimulus presentation and behavioral response quantification is computer automated, we argue that high-throughput screening for drugs or mutations that alter short-term memory performance of adult zebrafish is now becoming feasible.

Animated images as a tool to study visual communication: a case study in a cooperatively breeding cichlid

Investigating the role of visual information in animal communication often involves the experimental presentation of live stimuli, mirrors, dummies, still images, video recordings or computer animations. In recent years computer animations have received increased attention, as this technology allows the presentation of moving stimuli that exhibit a fully standardized behaviour. However, whether simple animated 2D-still images of conspecific and heterospecific stimulus animals can elicit detailed behavioural responses in test animals is unclear thus far. In this study we validate a simple method to generate animated still images using PowerPoint presentations as an experimental tool. We studied context-specific behaviour directed towards conspecifics and heterospecifics, using the cooperatively breeding cichlid Neolamprologus pulcher as model species. N. pulcher did not only differentiate between images of conspecifics, predators and herbivorous fish, but they also showed adequate behavioural responses towards the respective stimulus images as well as towards stimulus individuals of different sizes. Our results indicate that even simple animated still images, which can be produced with minimal technical effort at very low costs, can be used to study detailed behavioural responses towards social and predatory challenges. Thus, this technique opens up intriguing possibilities to manipulate single or multiple visual features of the presented animals by simple digital image-editing and to study their relative importance to the observing fish. We hope to encourage further studies to use animated images as a powerful research tool in behavioural and evolutionary studies.