Canine Sense and Sensibility: Tipping Points and Response Latency Variability as an Optimism Index in a Canine Judgement Bias Assessment

Recent advances in animal welfare science used judgement bias, a type of cognitive bias, as a means to objectively measure an animal''s affective state. It is postulated that animals showing heightened expectation of positive outcomes may be categorised optimistic, while those showing heightened expectations of negative outcomes may be considered pessimistic. This study pioneers the use of a portable, automated apparatus to train and test the judgement bias of dogs. Dogs were trained in a discrimination task in which they learned to touch a target after a tone associated with a lactose-free milk reward and abstain from touching the target after a tone associated with water. Their judgement bias was then probed by presenting tones between those learned in the discrimination task and measuring their latency to respond by touching the target. A Cox''s Proportional Hazards model was used to analyse censored response latency data. Dog and Cue both had a highly significant effect on latency and risk of touching a target. This indicates that judgement bias both exists in dogs and differs between dogs. Test number also had a significant effect, indicating that dogs were less likely to touch the target over successive tests. Detailed examination of the response latencies revealed tipping points where average latency increased by 100% or more, giving an indication of where dogs began to treat ambiguous cues as predicting more negative outcomes than positive ones. Variability scores were calculated to provide an index of optimism using average latency and standard deviation at cues after the tipping point. The use of a mathematical approach to assessing judgement bias data in animal studies offers a more detailed interpretation than traditional statistical analyses. This study provides proof of concept for the use of an automated apparatus for measuring cognitive bias in dogs.     

Effects of a chronic stress treatment on vaccinal response in lambs

Farming systems can expose animals to chronic mild stress which is known to induce negative affective state. Affective state in animals, as in humans, can be assessed through behavioral cues. This study aimed to describe the effect of a chronic mild stress, known to induce a negative affective state, on sheep health through their response to vaccination. The study used 15 lambs subjected to a model of chronic mild stress for 15 weeks and 15 lambs reared under conventional farming as a control group. After 7 weeks of stressful treatment, the lambs were individually exposed to a judgment bias test to assess a putative stress-induced ‘pessimism.’ After 15 weeks of stressful treatment, antibody immune response was measured after an injection of a live vaccine challenge (Chlamydia abortus attenuated vaccine strain 1B). Stressed lambs displayed a pessimistic-like perception in the judgment bias test, revealing a negative affective state. Stressed and control animals showed different immunological reactions to vaccine challenge: stressed sheep had lower hemoglobin concentrations and higher platelet, granulocyte and acute-phase protein concentrations. Antibody response induced by the vaccine strain was not different between stressed and control sheep. Our results suggest that negative affective state induced by chronic stress treatment may induce a stronger inflammatory response to vaccine challenge in sheep. Improvement of animal health may be achieved through consideration of stressors that may affect the emotional and immunological state of sheep.     

The Way Humans Behave Modulates the Emotional State of Piglets

The emotional state can influence decision-making under ambiguity. Cognitive bias tests (CBT) proved to be a promising indicator of the affective valence of animals in a context of farm animal welfare. Although it is well-known that humans can influence the intensity of fear and reactions of animals, research on cognitive bias often focusses on housing and management conditions and neglects the role of humans on emotional states of animals. The present study aimed at investigating whether humans can modulate the emotional state of weaned piglets. Fifty-four piglets received a chronic experience with humans: gentle (GEN), rough (ROU) or minimal contact (MIN). Simultaneously, they were individually trained on a go/no-go task to discriminate a positive auditory cue, associated with food reward in a trough, from a negative one, associated with punishments (e.g. water spray). Independently of the treatment (P = 0.82), 59% of piglets completed the training. Successfully trained piglets were then subjected to CBT, including ambiguous cues in presence or absence of a human observer. As hypothesized, GEN piglets showed a positive judgement bias, as shown by their higher percentage of go responses following an ambiguous cue compared to ROU (P = 0.03) and MIN (P = 0.02) piglets, whereas ROU and MIN piglets did not differ (P > 0.10). The presence of an observer during CBT did not modulate the percentage of go responses following an ambiguous cue (P > 0.10). However, regardless of the treatment, piglets spent less time in contact with the trough following positive cues during CBT in which the observer was present than absent (P < 0.0001). This study originally demonstrates that the nature of a chronic experience with humans can induce a judgement bias indicating that the emotional state of farm animals such as piglets can be affected by the way humans interact with them.     

Responses of mink to auditory stimuli: Prerequisites for applying the ‘cognitive bias’ approach

The aim of the study was to determine and validate prerequisites for applying a cognitive (judgement) bias approach to assessing welfare in farmed mink (Neovison vison). We investigated discrimination ability and associative learning ability using auditory cues. The mink (n = 15 females) were divided into two groups (High, n = 8; Low, n = 7, representing the frequency of the tone they were habituated to, 18 and 2 kHz respectively) and were tested using a habituation–dishabituation procedure in experiment 1. In experiment 2 one auditory stimulus was followed by an inter-trial-interval (safe/neutral situation), whereas another auditory stimulus was followed by an aversive stimulus (air blow) before the inter-trial-interval (danger situation). We observed behaviour including latencies to show a response during both experiments. The High mink showed significant habituation in experiment 1 but the Low mink only showed habituation in experiment 2. Regardless of the frequency used (2 and 18 kHz), cues predicting the danger situation initially elicited slower responses compared to those predicting the safe situation but quickly became faster. Using auditory cues as discrimination stimuli for female farmed mink in a judgement bias approach would thus appear to be feasible. However several specific issues are to be considered in order to successfully adapt a cognitive bias approach to mink, and these are discussed.     

Separation from the Dam Causes Negative Judgement Bias in Dairy Calves

Negative emotional states in humans are associated with a negative (pessimistic) response bias towards ambiguous cues in judgement tasks. Every mammalian young is eventually weaned; this period of increasing nutritional and social independence from the dam is associated with a pronounced behavioural response, especially when weaning is abrupt as commonly occurs in farm animals. The aim of the current study was to test the effect of separation from the cow on the responses of dairy calves in a judgement task. Thirteen Holstein calves were reared with their dams and trained to discriminate between red and white colours displayed on a computer monitor. These colours predicted reward or punishment outcomes using a go/no-go task. A reward was provided when calves approached the white screen and calves were punished with a timeout when they approached the red screen. Calves were then tested with non-reinforced ambiguous probes (screen colours intermediate to the two training colours). “GO” responses to these probes averaged (± SE) 72±3.6 % before separation but declined to 62±3.6 % after separation from the dam. This bias was similar to that shown by calves experiencing pain in the hours after hot-iron dehorning. These results provide the first evidence of a pessimistic judgement bias in animals following maternal separation and are indicative of low mood.     

Does Trapping Influence Decision-Making under Ambiguity in White-Lipped Peccary (Tayassu pecari)?

The white-lipped peccary (Tayassu pecari) is an endangered species whose bold anti-predator behaviour in comparison to related species may increase its vulnerability to hunting and predation. We used a judgement bias test to investigate whether captive peccaries that had recently experienced a trapping event made more ‘pessimistic’ decisions under ambiguity. If so, this would indicate (i) that the procedure may induce a negative affective state and hence have welfare implications, and (ii) that the species is able to adopt a cautious response style despite its bold phenotype. Eight individuals were trained to ‘go’ to a baited food bowl when a positive auditory cue (whistle; CS+) was given and to ‘no-go’ when a negative cue (horn A; CS-) was sounded to avoid a loud sound and empty food bowl. An ‘ambiguous’ auditory cue (bell; CSA) was presented to probe decision-making under ambiguity. Individuals were subjected to three tests in the order: T1 (control-no trap), T2 (24h after-trap procedure), and T3 (control-no trap). In each test, each animal was exposed to 10 judgement bias trials of each of the three cue types: CS+,CS-,CS_A. We recorded whether animals reached the food bowl within 60s (‘go’ response) and their response speed (m/s). The animals varied in their responses to the CS_A cue depending on test type. In all tests, animals made more ‘go’ responses to CS+ than CS_A. During control tests (T1 and T3), the peccaries showed higher proportions of ‘go’ responses to CS_A than to CS-. In T2, however, the animals showed similar proportions of ‘go’ responses to CS_A and CS-, treating the ambiguous cue similarly to the negative cue. There were differences in their response speed according to cue type: peccaries were faster to respond to CS+ than to CS- and CS_A. Trapping thus appeared to cause a ‘pessimistic’ judgement bias in peccaries, which may reflect a negative affective state with implications for the welfare and management of captive individuals, and also function to increase caution and survival chances following such an event in the wild environment.     

Leukocyte reactivity as an objective means of quantifying mental loading during ergonomic evaluation

Psychological stress evokes rapid changes to the cardiovascular and neuroendocrine systems, responses that can become habituated following repeated exposure. This study, comprising of two phases, suggests that the immune system follows a similar trend. Phase 1: 15 healthy subjects (aged between 26 and 56 years) provided capillary blood samples before and after completing three basic tasks using, in turn, two automotive touch screen interfaces (Interface 1—antecedent version, Interface 2—improved version). Using a chemiluminescent technique termed leukocyte coping capacity (LCC), the ability of leukocytes to produce reactive oxygen species in vitro was assessed. Significant differences in leukocyte activity were shown between treatment groups, where the greatest post-test decrease occurred after using Interface 1. Phase 2: a randomly selected sub-group (n = 4) underwent weekly repeat testing using both interfaces. Significant differences in post-test leukocyte reactivity were exhibited between test weeks for each interface—the magnitude of response decreasing with successive exposure.     

Looking on the bright side: biased attention and the human serotonin transporter gene

Humans differ in terms of biased attention for emotional stimuli and these biases can confer differential resilience and vulnerability to emotional disorders. Selective processing of positive emotional information, for example, is associated with enhanced sociability and well-being while a bias for negative material is associated with neuroticism and anxiety. A tendency to selectively avoid negative material might also be associated with mental health and well-being. The neurobiological mechanisms underlying these cognitive phenotypes are currently unknown. Here we show for the first time that allelic variation in the promotor region of the serotonin transporter gene (5-HTTLPR) is associated with differential biases for positive and negative affective pictures. Individuals homozygous for the long allele (LL) showed a marked bias to selectively process positive affective material alongside selective avoidance of negative affective material. This potentially protective pattern was absent among individuals carrying the short allele (S or SL). Thus, allelic variation on a common genetic polymorphism was associated with the tendency to selectively process positive or negative information. The current study is important in demonstrating a genotype-related alteration in a well-established processing bias, which is a known risk factor in determining both resilience and vulnerability to emotional disorders.     

Laughing Rats Are Optimistic

Emotions can bias human decisions- for example depressed or anxious people tend to make pessimistic judgements while those in positive affective states are often more optimistic. Several studies have reported that affect contingent judgement biases can also be produced in animals. The animals, however, cannot self-report; therefore, the valence of their emotions, to date, could only be assumed. Here we present the results of an experiment where the affect-contingent judgement bias has been produced by objectively measured positive emotions. We trained rats in operant Skinner boxes to press one lever in response to one tone to receive a food reward and to press another lever in response to a different tone to avoid punishment by electric foot shock. After attaining a stable level of discrimination performance, the animals were subjected to either handling or playful, experimenter-administered manual stimulation – tickling. This procedure has been confirmed to induce a positive affective state in rats, and the 50-kHz ultrasonic vocalisations (rat laughter) emitted by animals in response to tickling have been postulated to index positive emotions akin to human joy. During the tickling and handling sessions, the numbers of emitted high-frequency 50-kHz calls were scored. Immediately after tickling or handling, the animals were tested for their responses to a tone of intermediate frequency, and the pattern of their responses to this ambiguous cue was taken as an indicator of the animals'' optimism. Our findings indicate that tickling induced positive emotions which are directly indexed in rats by laughter, can make animals more optimistic. We demonstrate for the first time a link between the directly measured positive affective state and decision making under uncertainty in an animal model. We also introduce innovative tandem-approach for studying emotional-cognitive interplay in animals, which may be of great value for understanding the emotional-cognitive changes associated with mood disorders.     

The sky is falling: evidence of a negativity bias in the social transmission of information

The method of serial reproduction has revealed that the social transmission of information is characterized by the gradual transformation of the original message. This transformation results from the preferential survival of certain types of information and the resolution of ambiguity. Here we present evidence of a bias favoring the social transmission of negatively-valenced information across multiple transmission episodes. Ninety-two, four-person chains transmitted a story containing unambiguously positive and unambiguously negative story events, along with ambiguous story events that could be interpreted positively or negatively. Analysis using mixed-effects modeling revealed the preferential survival of unambiguously negative events over positive events, and the increasingly negative resolution of ambiguous events across successive transmission episodes. Contrary to predictions, elevated state anxiety did not enhance the social transmission of negatively-valenced information. We also found that the survival of unambiguously negative story events was positively correlated with the negative resolution of ambiguous story events, reflecting a general negativity-bias in the social transmission of information.     

Generalization and discrimination of positive and negative acoustic stimuli in the common carp (Cyprinus carpio)

Groups of common carp (Cyprinus carpio) were trained for 33 days to discriminate between two acoustic signals differing in frequency and temporal pattern. One signal (positive stimulus) was reinforced by food, while the other (negative stimulus) was not rewarded. When exposed to 3 positive and 3 negative stimuli per day (training Paradigm 1) the fish responded similarly to the two signals. When daily negative stimuli outnumbered positive stimuli (3 positive and 33 negative, training Paradigm 2) the fish responded similarly to the two signals for the first 2 weeks and then began to discriminate between them. Discriminatory response was statistically significant from Day 21 of training. After 33 days, training was switched from Paradigm 2 to Paradigm 1 and the fish maintained their discriminatory capability. The results are interpreted in terms of anticipatory frustration and risk management.     

Joyful by nature: approaches to investigate the evolution and function of joy in non-human animals

The nature and evolution of positive emotion is a major question remaining unanswered in science and philosophy. The study of feelings and emotions in humans and animals is dominated by discussion of affective states that have negative valence. Given the clinical and social significance of negative affect, such as depression, it is unsurprising that these emotions have received more attention from scientists. Compared to negative emotions, such as fear that leads to fleeing or avoidance, positive emotions are less likely to result in specific, identifiable, behaviours being expressed by an animal. This makes it particularly challenging to quantify and study positive affect. However, bursts of intense positive emotion (joy) are more likely to be accompanied by externally visible markers, like vocalisations or movement patterns, which make it more amenable to scientific study and more resilient to concerns about anthropomorphism. We define joy as intense, brief, and event-driven (i.e. a response to something), which permits investigation into how animals react to a variety of situations that would provoke joy in humans. This means that behavioural correlates of joy are measurable, either through newly discovered ‘laughter’ vocalisations, increases in play behaviour, or reactions to cognitive bias tests that can be used across species. There are a range of potential situations that cause joy in humans that have not been studied in other animals, such as whether animals feel joy on sunny days, when they accomplish a difficult feat, or when they are reunited with a familiar companion after a prolonged absence. Observations of species-specific calls and play behaviour can be combined with biometric markers and reactions to ambiguous stimuli in order to enable comparisons of affect between phylogenetically distant taxonomic groups. Identifying positive affect is also important for animal welfare because knowledge of positive emotional states would allow us to monitor animal well-being better. Additionally, measuring if phylogenetically and ecologically distant animals play more, laugh more, or act more optimistically after certain kinds of experiences will also provide insight into the mechanisms underlying the evolution of joy and other positive emotions, and potentially even into the evolution of consciousness.     

Diffusion Modelling Reveals the Decision Making Processes Underlying Negative Judgement Bias in Rats

Human decision making is modified by emotional state. Rodents exhibit similar biases during interpretation of ambiguous cues that can be altered by affective state manipulations. In this study, the impact of negative affective state on judgement bias in rats was measured using an ambiguous-cue interpretation task. Acute treatment with an anxiogenic drug (FG7142), and chronic restraint stress and social isolation both induced a bias towards more negative interpretation of the ambiguous cue. The diffusion model was fit to behavioural data to allow further analysis of the underlying decision making processes. To uncover the way in which parameters vary together in relation to affective state manipulations, independent component analysis was conducted on rate of information accumulation and distances to decision threshold parameters for control data. Results from this analysis were applied to parameters from negative affective state manipulations. These projected components were compared to control components to reveal the changes in decision making processes that are due to affective state manipulations. Negative affective bias in rodents induced by either FG7142 or chronic stress is due to a combination of more negative interpretation of the ambiguous cue, reduced anticipation of the high reward and increased anticipation of the low reward.     

Ovine IgA-reactive proteins from Teladorsagia circumcincta infective larvae

Infection of small ruminants with Teladorsagia circumcincta has, until now, been controlled using a combination of pasture management and frequent anthelmintic treatments. Resistance to the commonly used anthelmintics has driven research into the development of a subunit vaccine, encouraged by the demonstration of development of protective immunity in sheep following exposure to this parasite. Local immune effectors in the abomasum, in particular IgA, are thought to play important roles in naturally- and experimentally-acquired immunity. L3s represent the first contact of this pathogen with the host immune system and, herein, the presence of L3 antigen-specific IgA was demonstrated in abomasal mucus from immune sheep. This antibody source was used to immunoaffinity purify and identify IgA-reactive molecules present in L3s. We identified 155 different proteins in this way, including a number of activation-associated secretory proteins, venom allergen-like-type proteins, detoxifying enzymes, galectins and a suite of other potential vaccine candidate molecules. Levels of immunoaffinity-enriched L3 antigen-specific IgA in gastric lymph from previously-infected sheep were statistically significantly higher (P = 0.004) than those measured in helminth-free sheep and a statistically significant negative correlation (P = 0.005, r_s = −0.565) was identified between immunoaffinity-enriched L3 antigen-specific IgA levels in efferent gastric lymph and total T. circumcincta burden measured at necropsy. In addition, a statistically significant positive correlation (P = 0.007, r_s = 0.534) was measured between immunoaffinity-enriched L3 antigen-specific IgA levels in efferent gastric lymph and the percentage of inhibited L4s enumerated at necropsy. These results indicate that the purified antigens contain components that could be strongly considered as vaccine candidates.     

Toward a Choice-Based Judgment Bias Task for Horses

Judgment bias tasks for nonhuman animals are promising tools to assess emotional valence as a measure of animal welfare. In view of establishing a valid judgment bias task for horses, the present study aimed to evaluate 2 versions (go/no-go and active choice) of an auditory judgment bias task for horses in terms of acquisition learning and discrimination of ambiguous cues. Five mares and 5 stallions were randomly assigned to the 2 designs and trained for 10 trials per day to acquire different operant responses to a low-frequency tone and a high-frequency tone, respectively. Following acquisition learning, horses were tested on 4 days with 3 ambiguous-tone trials interspersed between the 10 high-tone and low-tone trials. All 5 go/no-go horses but only one active-choice horse successfully learned their task, indicating that it is more difficult to train horses on an active choice task than on a go/no-go task. During testing, however, go/no-go horses did not differentiate between the 3 different ambiguous cues, thereby making the validity of the test results questionable in terms of emotional valence.     

Mapping Proprioception across a 2D Horizontal Workspace

Relatively few studies have been reported that document how proprioception varies across the workspace of the human arm. Here we examined proprioceptive function across a horizontal planar workspace, using a new method that avoids active movement and interactions with other sensory modalities. We systematically mapped both proprioceptive acuity (sensitivity to hand position change) and bias (perceived location of the hand), across a horizontal-plane 2D workspace. Proprioception of both the left and right arms was tested at nine workspace locations and in 2 orthogonal directions (left-right and forwards-backwards). Subjects made repeated judgments about the position of their hand with respect to a remembered proprioceptive reference position, while grasping the handle of a robotic linkage that passively moved their hand to each judgement location. To rule out the possibility that the memory component of the proprioceptive testing procedure may have influenced our results, we repeated the procedure in a second experiment using a persistent visual reference position. Both methods resulted in qualitatively similar findings. Proprioception is not uniform across the workspace. Acuity was greater for limb configurations in which the hand was closer to the body, and was greater in a forward-backward direction than in a left-right direction. A robust difference in proprioceptive bias was observed across both experiments. At all workspace locations, the left hand was perceived to be to the left of its actual position, and the right hand was perceived to be to the right of its actual position. Finally, bias was smaller for hand positions closer to the body. The results of this study provide a systematic map of proprioceptive acuity and bias across the workspace of the limb that may be used to augment computational models of sensory-motor control, and to inform clinical assessment of sensory function in patients with sensory-motor deficits.     

Housing induced mood modulates reactions to emotional stimuli in sheep

The assessment of positive and negative short-term affective states (emotions) in animals and their modulation by long-term affective states (mood) is an on-going challenge. This study investigated the use of behavioural and physiological measures to assess emotions and their modulation by mood in sheep. To induce a more Positive and more Negative mood, two groups of sheep (n = 10 and 9) were kept under different housing conditions for 3 weeks. The Positive mood group was placed in a predictable environment rich in stimuli and with a calm human–animal interaction whereas sheep in the Negative mood group experienced a relatively barren and unpredictable environment with a harsher human–animal interaction. In the subsequent test week, 15 (8 and 7) experimental animals were exposed to four situations intended to elicit emotional reactions: separation from group members (negative valence), sham-grooming (low intensity negative), non-grooming (neutral), and grooming (positive valence). Data were tested for interactions between mood group and valence of the test situation using linear mixed models. More frequent ear-posture changes, a higher proportion of asymmetric ears, shorter inter-heartbeat intervals and higher respiration rates were observed during separation than during the other situations. Interactions between mood group and test situation showed that sheep in the Negative mood group reacted more negatively to the negative and more positively to the positive situation (proportion of asymmetric ears, inter-heartbeat interval, respiration rate). In conclusion, our findings suggest that sheep in a Positive mood reacted more weakly to an emotional situation independent of its valence, thus buffering negative events but also degrading positive events. In addition, this investigation showed the potential of using observations of ear postures and cardio-respiratory measures in sheep to assess the valence of short-term emotional states and their modulation by mood states.     

情绪信息的注意偏向研究

目的:考察被试对消极词和积极词在无意识状态下的注意偏向,探讨被试在无意识状态下对两类情绪词汇诱发的情绪信息所产生的注意选择与偏向问题。方法:以情绪词为材料,采用任务分离范式,考察被试在无意识状态下对情绪词汇的选择率和反应时。结果:(1)无意识注意阶段存在情绪刺激的注意偏向;(2)在选择率上,被试对积极词汇的选择要明显多于对中性词汇或消极词汇,且女性对积极词汇的选择率要明显高于男性;(3)在反应时上,被试对消极词汇的反应时要明显快于中性词汇或积极词汇。结论:该实验结果说明,带情绪信息的词汇都较中性词汇更能引起被试的注意偏向。     

SERT and uncertainty: serotonin transporter expression influences information processing biases for ambiguous aversive cues in mice

The long allele variant of the serotonin transporter (SERT, 5‐HTT) gene‐linked polymorphic region (5‐HTTLPR) is associated with higher levels of 5‐HTT expression and reduced risk of developing affective disorders. However, little is known about the mechanisms underlying this protective effect. One hypothesis is that 5‐HTT expression influences aversive information processing, with reduced negative cognitive bias present in those with higher 5‐HTT expression. Here we investigated this hypothesis using genetically‐modified mice and a novel aversive learning paradigm. Mice with high levels of 5‐HTT expression (5‐HTT over‐expressing, 5‐HTTOE mice) and wild‐type mice were trained to discriminate between three distinct auditory cues: one cue predicted footshock on all trials (CS+); a second cue predicted the absence of footshock (CS?); and a third cue predicted footshock on 20% of trials (CS20%), and was therefore ambiguous. Wild‐type mice exhibited equivalently high levels of fear to the CS+ and CS20% and minimal fear to the CS?. In contrast, 5‐HTTOE mice exhibited high levels of fear to the CS+ but minimal fear to the CS? and the CS20%. This selective reduction in fear to ambiguous aversive cues suggests that increased 5‐HTT expression reduces negative cognitive bias for stimuli with uncertain outcomes.