Does learning performance in horses relate to fearfulness, baseline stress hormone, and social rank?

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Abstract

The ability of horses to learn and remember new tasks is fundamentally important for their use by humans. Fearfulness may, however, interfere with learning, because stimuli in the environment can overshadow signals from the rider or handler. In addition, prolonged high levels of stress hormones can affect neurons within the hippocampus; a brain region central to learning and memory. In a series of experiments, we aimed to investigate the link between performance in two learning tests, the baseline level of stress hormones, measured as faecal cortisol metabolites (FCM), fearfulness, and social rank. Twenty-five geldings (2 or 3 years old) pastured in one group were included in the study. The learning tests were performed by professional trainers and included a number of predefined stages during which the horses were gradually trained to perform exercises, using either negative (NR) or positive reinforcement (PR). Each of the learning tests lasted 3 days; 7 min/horse/day. The NR test was repeated in a novel environment. Performance, measured as final stage in the training programme, and heart rate (HR) were recorded. Faeces were collected on four separate days where the horses had been undisturbed at pasture for 48 h. Social rank was determined through observations of social interactions during feeding. The fear test was a novel object test during which behaviour and HR were recorded.

Performance in the NR and PR learning tests did not correlate. In the NR test, there was a significant, negative correlation between performance and HR in the novel environment (rS = −0.66, P < 0.001, i.e. nervous horses had reduced performance), whereas there was no such correlation in the home environment (both NR and PR). Behavioural reactions in the fear test correlated significantly with performance in the NR test in the novel environment (e.g. object alertness and final stage: rS = −0.43, P = 0.04), suggesting that performance under unfamiliar, stressful conditions may be predicted by behavioural responses in a fear test. There was a negative correlation between social rank and baseline stress hormones (rS = −0.43, P = 0.04), i.e. high rank corresponded to low FCM concentrations, whereas neither rank nor FCM correlated with fearfulness or learning performance. We conclude that performance under stressful conditions is affected by activation of the sympathetic nervous system during training and related to behavioural responses in a standardised fear test. Learning performance in the home environment, however, appears unrelated to fearfulness, social rank and baseline FCM levels.

Introduction

Learning has been defined as a process of adaptive changes in individual behaviour as a result of experience (Thorpe, 1963). One type of learning is instrumental or operant conditioning, where a response made by the animal is followed by a biologically relevant event (reinforcement or punishment) that changes either the probability of the behaviour recurring or some aspect of its form (Mills et al., 2010). An aversive stimulus (punishment) reduces the likelihood of the action being repeated, whilst a desired consequence (reinforcement) increases the likelihood. Positive reinforcement is the addition of a pleasant stimulus to reward a desired response, whereas negative reinforcement is characterised by subtraction of an aversive stimulus (e.g. pressure) to reward a desired response and thus make this response more likely in the future (Mills et al., 2010). Some reviews have highlighted the paradox that most studies of equine learning are based only on positive reinforcement, whilst much traditional equine training is based on negative reinforcement (Cooper, 2007, Murphy and Arkins, 2007). Similarly, the majority of learning tests have investigated e.g. maze or discrimination learning with visual or spatial cues, whereas typical training techniques for horses are based on tactile or auditory cues. If learning studies are to be more applicable, it appears relevant to use tests which to a higher degree reflect how horses are trained in practise.

Some previous studies have reported that horses’ performance in different learning tests did not correlate (e.g. Lansade and Simon, 2010, Visser et al., 2003, Wolff and Hausberger, 1996). This lack of correlation between learning performance in different tests suggest that other characteristics, such as fearfulness, attention or motivation may govern success or failure in learning tests (Nicol, 2002). Increased learning by horses that are naturally calm may be due to reduced interference with the learning process, whereas fearful animals may shift attention away from the task, resulting in poor performance (Mendl, 1999, Nicol, 2002). Furthermore, fearfulness and stress may interfere with learning because prolonged high concentrations of glucocorticoids can impair both memory and learning skills as shown in several mammalian species; the link between stress hormones and these functional deficits is believed to relate to changes in the hippocampal formation (McEwen and Sapolsky, 1995, Morris, 2007). There is a large amount of scientific literature supporting the Yerkes-Dodson law, i.e. that cognitive function including learning has a biphasic relation (inverted U-shape) to stress levels; i.e. low or moderate concentrations of circulating glucocorticoids may enhance cognitive function, whilst high or prolonged elevations of these hormones can lead to cognitive disruption and performance below baseline levels (McEwen and Sapolsky, 1995, Mendl, 1999, Morris, 2007). Long-term stress of various housing or training conditions may therefore cause marked impairment of learning and memory abilities through the damaging actions of chronically elevated levels of glucocorticoids on brain structure.

In horses, no clear link between learning performance and fearfulness or stress has been demonstrated; Visser et al. (2003) indicated that emotionality, based on behavioural reactions during the learning test, may cause horses to be non-performers, whereas there was no simple relationship between heart rate, behaviour and learning performance in horses that did perform the task. Heird et al. (1986) found that emotionality, based on a subjective score of 1–4, did not correlate to maze test performance in 16 horses. They reported, however, that the least emotional horses (n not specified) ultimately achieved a higher level of performance. In contrast, Lansade and Simon (2010) found that fearfulness enhanced performance of ponies in an avoidance test based on positive punishment, but decreased performance in a negatively reinforced handling test. The handling test was, however, based on exercises (leading forward and backing) which the 36 participating 5–7 years old ponies that were accustomed to handling were likely to have experienced previously. The results may therefore reflect timing of reinforcement during previous handling rather than actual learning abilities.

There are to our knowledge no published studies of the effect of social status on fearfulness or baseline adrenocortical activity in horses, whereas some older studies failed to demonstrate effects of social dominance on learning in horses (reviewed by Nicol, 2002). We aimed to investigate learning performance in horses, evaluated through both positive and negative reinforcement in practical learning tests, and the link to fearfulness, baseline stress hormone levels as well as social status. The learning tests were developed in cooperation with professional trainers involving exercises that the young, participating horses had not previously experienced. We hypothesised that learning performance would be impaired by increased fearfulness and higher baseline stress hormone levels, which in turn would be influenced by social status.

Section snippets

Materials and methods

The study period was from July to October 2010. The study conformed to the ‘Guidelines for ethical treatment of animals in applied animal behaviour and welfare research’ by the ethics board of the International Society of Applied Ethology (www.applied-ethology.org).

Learning tests

An overview of results (HR and performance) from the three learning tests is presented in Table 3. In the NR test, the range in final training stage was 1.5–5, i.e. the horse that performed at the lowest level (H15) completed S1 and half of S2, whereas the horse with the highest performance (H17) completed S5. In the PR test, the range was 3 (H5)–5.75 (H6). The horses generally completed fewer stages in the NR test in the novel environment and the range was 0 (H8, H9) to 4 (H22). In both

Discussion

Our results demonstrate that performance in a practical learning test under unfamiliar and stressful conditions can be predicted by behavioural reactions in a standardised fear test, performed in the home environment. The reported reactions in the novel object test were strongly correlated to reactions in three other types of fear tests, including exposure to sudden and tactile stimuli (Christensen, under review), suggesting that the responses reflected an underlying trait. Thus the

Acknowledgements

We kindly acknowledge the horse owners for allowing us to use their horses and Susan Kjærgaard, BlueBerryHill, Denmark, for training the horses. This study was funded by the Danish Research Council for Technology and Production.

References (32)

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