Léa Lansade

Towards an Ethological Animal Model of Depression? A Study on Horses

Background Recent reviews question current animal models of depression and emphasise the need for ethological models of mood disorders based on animals living under natural conditions. Domestic horses encounter chronic stress, including potential stress at work, which can induce behavioural disorders (e.g. “apathy”). Our pioneering study evaluated the potential of domestic horses in their usual environment to become an ethological model of depression by testing this models’ face validity (i.e. behavioural similarity with descriptions of human depressive states). Methodology/Principal Findings We observed the spontaneous behaviour of 59 working horses in their home environment, focusing on immobility bouts of apparent unresponsiveness when horses displayed an atypical posture (termed withdrawn hereafter), evaluated their responsiveness to their environment and their anxiety levels, and analysed cortisol levels. Twenty-four percent of the horses presented the withdrawn posture, also characterized by gaze, head and ears fixity, a profile that suggests a spontaneous expression of “behavioural despair”. When compared with control “non-withdrawn” horses from the same stable, withdrawn horses appeared more indifferent to environmental stimuli in their home environment but reacted more emotionally in more challenging situations. They exhibited lower plasma cortisol levels. Withdrawn horses all belonged to the same breed and females were over-represented. Conclusions/Significance Horse might be a useful potential candidate for an animal model of depression. Face validity of this model appeared good, and potential genetic input and high prevalence of these disorders in females add to the convergence. At a time when current animal models of depression are questioned and the need for novel models is expressed, this study suggests that novel models and biomarkers could emerge from ethological approaches in home environments.

Stress Modulates Instrumental Learning Performances in Horses (Equus caballus) in Interaction with Temperament

The present study investigates how the temperament of the animal affects the influence of acute stress on the acquisition and reacquisition processes of a learning task. After temperament was assessed, horses were subjected to a stressor before or after the acquisition session of an instrumental task. Eight days later, horses were subjected to a reacquisition session without any stressor. Stress before acquisition tended to enhance the number of successes at the beginning of the acquisition session. Eight days later, during the reacquisition session, contrary to non-stressed animals, horses stressed after acquisition, and, to a lesser extent, horses stressed before acquisition, did not improve their performance between acquisition and reacquisition sessions. Temperament influenced learning performances in stressed horses only. Particularly, locomotor activity improved performances whereas fearfulness impaired them under stressful conditions. Results suggest that direct exposure to a stressor tended to increase acquisition performances, whereas a state of stress induced by the memory of a stressor, because it has been previously associated with the learning context, impaired reacquisition performances. The negative effect of a state of stress on reacquisition performances appeared to be stronger when exposure to the stressor occurred after rather than before the acquisition session. Temperament had an impact on both acquisition and reacquisition processes, but under stressful conditions only. These results suggest that stress is necessary to reveal the influence of temperament on cognitive performances.

Behavioral and Transcriptomic Fingerprints of an Enriched Environment in Horses (Equus caballus).

The use of environmental enrichment (EE) has grown in popularity over decades, particularly because EE is known to promote cognitive functions and well-being. Nonetheless, little is known about how EE may affect personality and gene expression. To address this question in a domestic animal, 10-month-old horses were maintained in a controlled environment or EE for 12 weeks. The control horses (n = 9) lived in individual stalls on wood shaving bedding. They were turned out to individual paddocks three times a week and were fed three times a day with pellets or hay. EE-treated horses (n = 10) were housed in large individual stalls on straw bedding 7 hours per day and spent the remainder of the time together at pasture. They were fed three times a day with flavored pellets, hay, or fruits and were exposed daily to various objects, odors, and music. The EE modified three dimensions of personality: fearfulness, reactivity to humans, and sensory sensitivity. Some of these changes persisted >3 months after treatment. These changes are suggestive of a more positive perception of the environment and a higher level of curiosity in EE-treated horses, explaining partly why these horses showed better learning performance in a Go/No-Go task. Reduced expression of stress indicators indicated that the EE also improved well-being. Finally, whole-blood transcriptomic analysis showed that in addition to an effect on the cortisol level, the EE induced the expression of genes involved in cell growth and proliferation, while the control treatment activated genes related to apoptosis. Changes in both behavior and gene expression may constitute a psychobiological signature of the effects of enrichment and result in improved well-being. This study illustrates how the environment interacts with genetic information in shaping the individual at both the behavioral and molecular levels.

Dimensions of Temperament Modulate Cue-Controlled Behavior: A Study on Pavlovian to Instrumental Transfer in Horses (Equus Caballus)

Pavlovian to instrumental transfer (PIT) is a central factor in how cues influence animal behavior. PIT refers to the capacity of a Pavlovian cue that predicts a reward to elicit or increase a response intended to obtain the same reward. In the present study, using an equine model, we assessed whether PIT occurs in hoofed domestic animals and whether its efficacy can be modulated by temperamental dimensions. To study PIT, horses were submitted to Pavlovian conditioning whereby an auditory–visual stimulus was repeatedly followed by food delivery. Then, horses were submitted to instrumental conditioning during which they learned to touch with their noses an object signaled by the experimenter in order to obtain the same reward. During the PIT test, the Pavlovian conditioned stimulus was presented to the animal in the absence of reward. At the end of the experiment, a battery of behavioral tests was performed on all animals to assess five temperamental dimensions and investigate their relationships with instrumental performance. The results indicate that PIT can be observed in horses and that its efficacy is greatly modulated by individual temperament. Indeed, individuals with a specific pattern of temperamental dimensions (i.e., higher levels of gregariousness, fearfulness, and sensory sensitivity) exhibited the strongest PIT. The demonstration of the existence of PIT in domesticated animals (i.e., horses) is important for the optimization of its use by humans and the improvement of training methods. Moreover, because PIT may be implicated in psychological phenomena, including addictive behaviors, the observation of relationships between specific temperamental dimensions and PIT efficacy may aid in identifying predisposing temperamental attributes.

Characterization of long-term memory, resistance to extinction, and influence of temperament during two instrumental tasks in horses

The present study investigated the influence of temperament on long-term recall and extinction of 2 instrumental tasks in 26 horses. In the first task (backward task), horses learned to walk backward, using commands given by an experimenter, in order to obtain a food reward. In the second task (active avoidance task), horses had to cross an obstacle after a bell rang in order to avoid emission of an air puff. Twenty-two months after acquisition, horses exhibited perfect recall performance in both tasks. Accordingly, no influence of temperament on recall performance could be observed for either task. In contrast, in the absence of positive or negative outcomes, the horses’ ability to extinguish their response to either task was highly variable. Resistance to extinction was related to some indicators of temperament: The most fearful horses tended to be the most resistant to extinction in the backward task, while the least sensitive horses tended to be the most resistant to extinction in the active avoidance task. These findings reveal extensive long-term memory abilities in horses and suggest an influence of temperament on learning processes other than acquisition.

Stress affects instrumental learning based on positive or negative reinforcement in interaction with personality in domestic horses

The present study investigated how stress affects instrumental learning performance in horses (Equus caballus) depending on the type of reinforcement. Horses were assigned to four groups (N = 15 per group); each group received training with negative or positive reinforcement in the presence or absence of stressors unrelated to the learning task. The instrumental learning task consisted of the horse entering one of two compartments at the appearance of a visual signal given by the experimenter. In the absence of stressors unrelated to the task, learning performance did not differ between negative and positive reinforcements. The presence of stressors unrelated to the task (exposure to novel and sudden stimuli) impaired learning performance. Interestingly, this learning deficit was smaller when the negative reinforcement was used. The negative reinforcement, considered as a stressor related to the task, could have counterbalanced the impact of the extrinsic stressor by focusing attention toward the learning task. In addition, learning performance appears to differ between certain dimensions of personality depending on the presence of stressors and the type of reinforcement. These results suggest that when negative reinforcement is used (i.e. stressor related to the task), the most fearful horses may be the best performers in the absence of stressors but the worst performers when stressors are present. On the contrary, when positive reinforcement is used, the most fearful horses appear to be consistently the worst performers, with and without exposure to stressors unrelated to the learning task. This study is the first to demonstrate in ungulates that stress affects learning performance differentially according to the type of reinforcement and in interaction with personality. It provides fundamental and applied perspectives in the understanding of the relationships between personality and training abilities.

Personality and predisposition to form habit behaviours during instrumental conditioning in horses (Equus caballus)

The relationship between personality and learning abilities has become a growing field of interest. Studies have mainly focused on the relationship with performance, such as the speed of acquisition. In this study, we hypothesised that personality could in part also be related to a certain predisposition of an individual to switch more easily from a goal-directed process to a habit process during learning. To identify these processes, we conducted a contingency degradation protocol. This study investigated 1/ whether in general horses are able to adjust their response according to the contingency between their action and the reward, 2/ whether there are any relationships between certain personality profiles and a predisposition to switch more rapidly to habitual processes, and 3/ whether emotional states experienced during the learning procedure play a role in this switching. Personality tests were conducted on 29 horses, followed by a degradation contingency protocol. Overall, results show that horses were sensitive to contingency degradation between their action and the reward. Nevertheless, there was inter-individual variability: the horses presenting high fearfulness, and to a lesser extent low sensory sensitivity and low gregariousness were less sensitive to the degradation, demonstrating that they were more likely to switch to a habitual process. Contrary to our expectations, the emotional state experienced during the procedure did not seem to explain this switching. We conclude that personality is not only related to learning performance, but also in part to the process involved during learning, independently of the emotion experienced during the process. This study provides new theoretical knowledge on cognitive skills in ungulates.

Facial display and blushing: Means of visual communication in blue-and-yellow macaws (Ara Ararauna)?

Mainly recognized for their cognitive performance, the visual communication system and, particularly, the potential function of facial displays in parrots remain thus far unexplored. Here, we provide the first descriptive study of facial display use in captive blue-and-yellow macaws. We observed the feather position (sleeked or ruffled) on the crown, nape and cheek at the group level during the macaws’ daily routine and individually while interacting with a familiar animal caretaker. In the latter context, blushing was also assessed on the bare skin of the cheek. Group level observations showed that crown, nape and cheek feathers ruffling was more frequent in activities requiring no locomotion than in activities requiring locomotion. With the animal caretaker, crown ruffling was significantly more frequent when the caretaker was actively engaging with the parrot than during a control phase with no mutual interaction. In addition, a significantly higher proportion of naïve observers judged blushing as being present on photographs taken during the mutual interaction phase than during the control phase. We thus showed significant variations in facial displays and bare skin colour based on the birds’ social context and activity. Our results broaden the scope for further studies to determine whether parrots’ faces provide visual social signals.

Are there facial indicators of positive emotions in birds? A first exploration in Japanese quail

The positive aspect of emotions, like pleasure, remains overlooked in birds. Our aim was to contribute to the exploration of facial indicators of positive emotions. To observe contrasting emotional expressions, we used two lines of Japanese quail divergently selected on their inherent fearfulness: a fearful line (long tonic immobility duration: LTI) and a less fearful line (short tonic immobility duration: STI). To induce positive emotions, we gave individual quail the opportunity to perform a rewarding behaviour, dustbathing, in an unfamiliar cage. More STI than LTI quail expressed dustbathing and latencies to dustbathe were significantly shorter in STI than LTI quail. This result indicated that the lines of quail differed in their fearfulness of the situation. We observed crown feather height, throat feather angle and pupil surface before (control) and during dustbathing. We found significant increases in crown feather height, pupil area and angle of throat feathers between the control and the dustbathing phases in STI quail, and pupil area correlated positively with crown feather height. In LTI quail, the angle of throat feathers increased during dustbathing, but the other parameters did not differ. We argue that variation in crown feather height and pupil area may provide indications of positive emotions in Japanese quail.

A trait for a high emotionality favors spatial memory to the detriment of cue-based memory in Japanese quail

Recent studies provided evidence that a personality trait such as a trait for a high or a low emotionality can either promotes or impairs learning and memory performances. This variability can be partly explained because this trait may have opposite effect on memory performances depending on the memory system involved. The present study investigated in Japanese quail the relationships between emotionality and two forms of memory, spatial- memory and cue-based memory. We showed that birds with a high emotionality trait (E+), compared with birds with a low emotionality trait (E-), reached slowly but more accurately the spatial location of a rewarded cup in an arena that contains 8 identical cups. Then a second cohort of E + and E- quails was trained to solve a dual spatial/cued task in which they could use either their spatial or cue-based memory. Whereas E + birds predominantly solved the task using their spatial memory, E- birds preferentially used their cue-based memory. These findings demonstrate that a trait for a high emotionality, can influence spatial memory performances but also contributes to favor the selection of this form of memory.