Behavioural Processes 76 (2007) 1–13 Review Equine learning behaviour Jack Murphy ∗ , Sean Arkins Department of Life Sciences, University of Limerick, Limerick, Ireland Received 14 June 2006; accepted 15 June 2006 Abstract Scientists and equestrians continually seek to achieve a clearer understanding of equine learning behaviour and its implications for training. Behavioural and learning processes in the horse are likely to influence not only equine athletic success but also the usefulness of the horse as a domesticated species. However given the status and commercial importance of the animal, equine learning behaviour has received only limited investigation. Indeed most experimental studies on equine cognitive function to date have addressed behaviour, learning and conceptualisation processes at a moderately basic cognitive level compared to studies in other species. It is however, likely that the horses with the greatest ability to learn and form/understand concepts are those, which are better equipped to succeed in terms of the human–horse relationship and the contemporary training environment. Within equitation generally, interpretation of the behavioural processes and training of the desired responses in the horse are normally attempted using negative reinforcement strategies. On the other hand, experimental designs to actually induce and/or measure equine learning rely almost exclusively on primary positive reinforcement regimes. Employing two such different approaches may complicate interpretation and lead to difficulties in identifying problematic or undesirable behaviours in the horse. The visual system provides the horse with direct access to immediate environmental stimuli that affect behaviour but vision in the horse is of yet not fully investigated or understood. Further investigations of the equine visual system will benefit our understanding of equine perception, cognitive function and the subsequent link with learning and training. More detailed comparative investigations of feral or free-ranging and domestic horses may provide useful evidence of attention, stress and motivational issues affecting behavioural and learning processes in the horse. The challenge for scientists is, as always, to design and commission experiments that will investigate and provide insight into these processes in a manner that withstands scientific scrutiny. © 2007 Elsevier B.V. All rights reserved. Keywords: Horse; Behaviour; Learning; Processes; Memory Contents 1. 2. 3. 4. 5. 6. 7. 8. 9. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 Learning processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Learning ability and intelligence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3.1. Comparative studies of animal intelligence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Memory in the horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Experimental task learning and behaviour in the horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5.1. Experimental testing of equine learning and behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 5.2. Horses experience learning difficulties due to temporal delays . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 5.3. Maze learning trials in the horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 5.4. Sidedness could influence learning and behaviour in the horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Social and observational learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Attempts at assessing higher order cognition in horses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Learning and behaviour in the feral horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Contemporary training schemes and equine learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10 ∗ Corresponding author. Present address: School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, 206 Veterinary Sciences Building, Belfield, Dublin 4, Ireland. Tel.: +353 87 284 3070; fax: +353 1 7166104. E-mail address: Jack.Murphy@ucd.ie (J. Murphy). 0376-6357/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2006.06.009 2 J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 10. Cellular and molecular basis of equine learning behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction The horse has evolved through domestication to adapt to man and the environment he provides (Price, 1999). Adaptation to domestication in any of the animal species has been largely dependant on the degree of developmental plasticity of the animal and the typical behavioural and learning patterns compatible with the husbandry techniques utilised during the domestication process (Price, 1999). Neurobiological and behavioural factors influence several aspects of equine learning and ultimately athletic ability and success in the horse (Visser et al., 2003). It is likely that the horses with the greatest ability to understand or conceptualise are those, which are better equipped to deal with the demands of contemporary and future training schemes. There is also general consensus among scientists and lay practitioners that equine training regimes and welfare programmes associated with the horse should continually strive to match the complexity, levels of comprehension and learning intensity that is innate to the horse. However, even with the importance attributed to the role of the horse in human society, it has been reported that surprisingly little scientific research has addressed the issue of equine learning and its implications (Nicol, 2002). Historically, difficulties have arisen with the elucidation of many equine learning and behavioural processes and some notable inconsistencies regarding terminology and the interpretation of subsequent equine behaviour have been reported (Mills, 1998a,b). In an attempt to appraise and categorise equine behavioural terminology and its meanings, this inconsistency in terminology issue has been recently addressed and as a result more helpful ethograms detailing inventories of specific behaviours in the horse have been completed (McDonnell and Poulin, 2002). Nevertheless, even following further attempts at producing unequivocal descriptive terminology and definitive analysis of equine behaviour and learning processes, some difficulties with interpretation still remain (McGreevy et al., 2005). This situation may lead to a lack of rigor in attempting to identify and control problem behaviours in the horse. However, equine ethology and investigation of equine behaviour under experimental conditions are subject areas of research that are currently becoming more popular under a number of general categories. The areas of interest that have been targeted for detailed investigative research in the horse include: learning, training, feral behaviour, stereotypies, breeding behaviour and temperament assessment (Houpt and Rudman, 2002). The primary goal, for those interested in equine behavioural and learning processes in the horse, and how this affects human–horse relationships, should be to maximise the potential benefits for both man and animal. One of the very earliest acknowledged authorities, Xenophon, ca. 400 bc declared that ‘what we need is that the horse should of its ‘own accord’ exhibit his finest airs and paces at set signals. . . such are the horses on 10 10 10 which gods and heroes ride’ (Rees, 1997). While Xenophon referred to the outward expression of athleticism in the horse, one inference is that the horse would also learn and perhaps more importantly understand the signals involved in requesting such behavioural demonstrations in its association with man. Whereas human interaction with the horse and the domestication process have been of enormous benefit to the horse in terms of veterinary care, protection and survival, some potential disadvantages and conflicting practices have also developed in tandem. Because of mans’ often insensitive selection techniques and modern training regimes, the resulting social isolation and the restricted breeding opportunities have regularly been at variance with the evolutionary processes of the ancestors of the modern horse (Goodwin, 1999). A more detailed understanding of these conflicting practices would help to promote improved equine management interactions and in so doing would likely maximise man’s appreciation of behavioural and learning processes in the horse. Humans have regularly attempted to reinforce dominance strategies on the horses in their care in an attempt to elicit the desired outcomes and responses from the animals (Creigier, 1987). This may be a misguided strategy given that the natural equine response to dominance is likely to be one of avoidance and it has recently been shown that training is actually enhanced when the training methods employed exactly match the mental ability of the horse (McLean and McGreevy, 2004). While their methods may not always have been based on scientific research, some informed trainers have highlighted the importance of a better understanding and appreciation of equine behavioural and learning processes (Roberts, 1996). Given this raised awareness and apparent benefit, it is likely that learning behaviour and the horse–human relationship might be aptly modified with the imposition of a better balanced social interaction between horse and human (Goodwin, 1999). Several other conditions affecting equine learning behaviour have been reported to induce fearfulness in the horse including isolation from conspecifics, exposure to novel objects or novel conditions and, under certain circumstances, proximity to humans (Lansade et al., 2004). It has been reported that early handling has particularly positive behavioural effects in animals and it has been shown to reduce animals’ fear of humans, while high levels of fearfulness have certainly been shown to impair learning ability in the horse (Fiske and Potter, 1979). Although foal imprint training has been promoted in the equine industry, there are only limited documented scientific studies available regarding this form of training or its efficacy. In one such study Williams et al. (2002) actually concluded that there was no difference between foals at three months of age between controls (foals on pasture without training) and trained foals (following a three month programme) and therefore, imprint training appeared to have limited effect on the foals J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 as a result. In a longitudinal study, with respect to early training on the jumping technique of horses, Santamaria et al. (2005) concluded that specific training for jumping at an early age was unnecessary because effects on both technique and jumping capacity was only temporary in nature. Nonetheless further scientific evaluation of handling, apparent beneficial effects of training and interpretation of learning processes in the horse is necessary and will be welcomed. 2. Learning processes Within the current human–horse relationship, the horse is primarily involved in a wide variety of sporting and leisure time activities (Lansade et al., 2004), and is the basis for an industry of considerable commercial importance (Giulotto, 2001). Curiously however, given the long association between man and horse, there currently exists only minimal published scientific research with regard to equine learning and comprehension (Nicol, 2002). Learning has been described as changes in an animal’s behaviour resulting from experience of some condition or set of circumstances (Tarpey, 1975; Chance, 1993). However, while learning represents modification to the internal behavioural organisation of any species, the process depends on the reinforcing properties or experience of the species’ environment (Domjan and Burkhard, 1986). Additionally, learning can be described as either an active or a passive occurrence, and working descriptions of what learning actually is vary only slightly. In any event, the processes of both active and passive leaning behaviours always involve experience – the experience of learning some phenomenon. Mackintosh (1983) reported that learning could be sub-divided into three broad forms that might be considered important in relation to general training procedures. The broad forms include: (i) non-associative learning, typically habituation and sensitisation, (ii) associative learning or conditioning and (iii) complex learning or insight. It has also been generally accepted from a psychological perspective, that learning typically follows a series of incremental stages of (a) exposure to a stimulus, (b) acquisition of a response behaviour, (c) fluency, (d) generalisation and (e) subsequent maintenance of the learned response with sustained reliability even under various settings. In terms of learning behaviour, no evidence has as of yet been produced to suggest that horses actually learn any differently than do any other species (Mills, 1998a,b). Learning behaviour in any species is also critically influenced by the timing of exposure to the stimulus and introduction of the associated reinforcement strategy. Experienced handlers have been astutely aware of the necessity to apply reinforcement schedules immediately or as close as possible to the demonstration of the desired behaviour in the horse for optimal effect. This concept is also the basis for Pavlovian (classical) and operant (instrumental) learning (Bouton and Swartzentruber, 1991). Operant learning or conditioning is a training technique employed within several aspects of equestrianism (Cooper, 1998). Scientific research in this area of equine learning is relatively sparse to date, but it is certainly warranted (Miyashita et al., 2000; McLean, 2001; Williams et 3 al., 2004). Training and subsequent learning in the horse are particularly aggravated by delayed, conflicting or meaningless cues and reinforcements. Hull (1943) showed that the application of two intensive stimuli simultaneously would result in ‘blocking’, where neither correct response would be learned. This is an important issue regarding learning and training for the horse as Wiepkema (1987) has indicated that conflict behaviours such as ambivalent, redirected and displacement behaviour result from unpredictability in the stimulus–response relationship employed during animal training. With regard to the efficacy of training, repetitions, temporal distribution and duration of training schedules and exposure to the test stimuli have been investigated experimentally in the horse. In general, the findings of such experimental trials have concluded that extended sessions of concentrated training schedules produces inappropriate and inefficient learning behaviour in the horse (Rubin et al., 1980; McCall, 1990; Sappington et al., 1997). Indeed, following a substantive review, Nicol (2002) reported that there was poor correlation between learning behaviour in individual horses and the subsequent performance of the same horses during different experimental tasks. At best it appeared that learning behaviour was a function of the individual horse and any correlation with performance levels in subsequent experimental trials was very much dependant upon the specific task involved. This is interesting, particularly when considering earlier work suggesting that behavioural and learning characteristics observed in foals were not only heritable but that the subsequent performance features of the animals could be predicted from observations of pre-weaning behaviour of the foals (Wolff and Hausberger, 1994). The inference from the Wolff and Hausberger (1994) study was that progeny of certain sires appeared to exhibit similar behavioural displays in their play patterns and other spatial interactions with their dams. With regard to dealing with young horses, this might be important when training similarly bred horses and predicting how they might learn and react to certain stimuli. 3. Learning ability and intelligence There is enormous difficulty in assessing intelligence levels within and between all animals, primarily because of the difficulties in asserting what actually constitutes intelligence per se. Many of the earliest attempts at comparative psychology have postulated that intelligence and learning behaviour were intrinsically linked to or based on a ‘scalae naturae’ or so called ladder of life (Hodos and Campbell, 1969). The ladder system placed species in a hierarchical order with humans at the top of the ladder in terms of intelligence and learning ability and transcended downwards through a level including apes, monkeys and dolphins to further groupings of dogs, cats rat, birds, reptiles, fish and amphibians and finally leading to a basal level of insects (Linnaeus, 1758). However, numerous attempts at applying this ‘order format’ to animal learning ability and intelligence assessment across species have received repeated criticism to such an extent that it has been labelled as no longer valid (Hodos and Campbell, 1969; Houpt, 1979; Mackintosh, 1988). The difficulty lies not least in 4 J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 Table 1 Hierarchy of learning abilities Level Hierarchy of learning abilities (adapted from Thomas, 1986) (1) Habituation (2) Classical conditioning (3) Simple operant conditioning (4) Chaining operant responses (5) Concurrent discriminations (6) Concept learning (7) Conjunctive, disjunctive and conditional concepts (8) Biconditional concepts Description Learning not to respond to a repeated stimulus that has no consequences Making reflex responses to a new stimulus that has been repeatedly paired with the original innate stimulus Learning to repeat a voluntary response to obtain reinforcement Learning a connected sequence of operant responses to obtain reinforcement Learning to make an operant response to only one set of stimuli for more than one set of stimuli concurrently applied Discrimination learning based on some common characteristic shared by a number of stimuli Learning of concept involving a relationship between stimuli of the forms ‘A and B’, ‘A or B’, and ‘If A then B’, respectively Learning of concept involving complex logical reasoning, such as ‘A if and only if B’ designing an appropriate experimental situation or trial, to test a range of species in a manner, whereby the experimental design does not bias the result in favour of one or more of the species under investigation. However, Thomas (1986) produced an interesting hierarchy of learning skills ranging from purely basic habituation to complex logical reasoning. This matrix pointed towards an index of intelligence levels by determining relative position within the hierarchy of the learning skills at which an animal was capable of performing (Table 1). Thomas (1986) compiled results based on experimental trials demonstrating the ability for concurrent discrimination in various fish, reptiles, birds, and mammals, including mice, rats, zebras, donkeys, horses and elephants. The results appeared to suggest that of all the species tested; only the elephant was capable of successfully completing as many concurrent discrimination tasks as the horse (level 5; Table 1). Earlier equine learning research had shown that basic discrimination, memory and learning behaviour in the horse was very good (Giebel, 1958; Dixon, 1970; Houpt, 1979). On the other hand Sappington et al. (1997) concluded that equine learning between simple discrimination tasks was poorly correlated. In addition, it has also been reported that performance under one set of experimental conditions were not necessarily predictive of similar performance levels involving different experimental conditions (Sappington et al., 1997; Nicol, 2002). 3.1. Comparative studies of animal intelligence Davis and Cheeke (1998) declared intelligence and learning ability in the horse relative to other species was the subject of some considerable speculation, particularly on an anecdotal level. While it has been reported that horses are less than intellectual giants among domestic animals, they have been selected not only for muscle mass and speed but also specifically for trainability (Houpt, 1979). Trainability and intellect are of considerable importance and are highly influential when considering the requirement for horses to respond to subtle stimuli in various disciplines of equitation (Visser et al., 2003). One of the most famous examples of highly intelligent equine responsiveness or perception was undoubtedly the early 20th century German horse Clever Hans, whose owner actually believed that the horse was capable of solving various mathematical problems by numerically tapping out correct answers with a fore-limb. Rather than possess a proficiency in the calculations, the horse had very astutely learned to interpret extremely subtle stimuli from unsuspecting but participating (and anticipating) audiences (Budiansky, 1997). Further cross species comparisons have indicated that horses were capable of making better discriminations than sheep, zebras or donkeys. Furthermore, while horses remembered what they learned, though not as well as cows, they learned to avoid pain by running or jumping and were faster to achieve this than pigs, but not as quick as dogs (Houpt, 1979). In general, horses tend to perform poorly in tests based on food tasting and food aversion. While rats and pigs, easily learned to refrain from eating sweet feeds, which had poisonous consequences, horses did not seem to have this learning ability (Houpt, 1979). Although their consummatory behaviour is often based on large infrequent meals, carnivores also have the ability to form food and/or taste aversions. In one study where illness was associated with the consumption of a relatively novel feed (induced by apomorphine administration immediately following consumption) ponies demonstrated the ability to form an aversion to a novel feed under some conditions (Houpt et al., 1990). However, during trials where apomorphine administration was delayed for 30 min following ingestion of the feed, the ponies were unable to associate the illness with the consumption of discrete feeds (Houpt et al., 1990). As a consequence horses are likely to be exposed to poisonous and toxic challenge because of the inability to learn specific feed aversions in situations where illness is delayed. This is particularly the case following consumption of long-acting toxins associated with some plant species such as Senecio and Equistrium (Oehme, 1987). This apparent learning difficulty could be due to differences in feeding behaviour in the species. Horses are natural trickle feeders and as such, may find it more difficult than some other species to distinguish discrete feeds, which could harbour or be associated with detrimental effects following ingestion. This scenario highlights another issue that warrants further investigation in terms of learning and intelligence in the horse. In terms of differences among species, it was also previously suggested, that the ratio of the brain to body weight was the best J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 measure of intelligence (Jerison, 1973). However, it has been subsequently demonstrated that this method also falls short as a critical index or measurement technique for intelligence during comparisons of animals of very different size (Houpt, 1979). Relative species intelligence ranking may prove at best questionable, even though horse owners in particular, often speculate how intelligent horses are in relation to other animals (McDonnell, 2001). Moreover, idiosyncrasies in animal behaviour probably reflect a range of sensations actually experienced by the animal species under investigation and this issue needs to be better understood in order to definitively evaluate animal intelligence. Nonetheless McLean (2001) suggested that current experimental methods should be extended to a greater diversity of species, and that innovative experiments should also be designed to test for specific cognitive function in all groups of animals including the horse. 4. Memory in the horse While it is generally accepted that memory is the function of encoded neural connections, there is as yet no universally agreed model of how memory specifically works (Schacter, 1996). Wolff and Hausberger (1996) reported that equine learning and memorisation did not appear to be linked following simple experimental discrimination and spatial discrimination tasks and concluded that learning and memory in the horse, at least, may involve different processes. Nicol (2002) reported that many examples of excellent memory and recall ability have been documented in the horse. It does appear however, that the extent of memory can be easily taken for granted and that assumptions about memory in the horse are often made without knowing the basis for such assumptions. Indeed there is scarcely an animal behaviour that is not affected by memory to some degree. In one study, horses proved themselves capable of remembering and repeating a learned response after an interval of 1 week under experimental maze conditions (Marinier and Alexander, 1994). In another study based on a spatial task requirement, foals learned and remembered very well when they were exposed to identical wall mounted compartments to locate food (Mal et al., 1993). The achievement of successful learning and memory outcomes is likely to be extremely important in the human–horse relationship and contemporary training programmes. Given the reports of excellent memory in the horse, it is perhaps somewhat surprising that recent equine short-term spatial memory research has suggested that horses may have limitations in recall ability. Specifically, horses may not have a prospective type of memory, particularly in relation to temporal delays during exposure to stimuli (McLean, 2004a). This may be of crucial importance in equitation and all other forms of training associated with the horse and it is an issue that will no doubt invite further investigation. Notwithstanding the difficulty that any form of temporal delay may present for the horse, it would appear that the more a horse’s brain is stimulated in terms of memory recall, the quicker the learning of new experiences occurs (Hanggi, 1999). It is equally likely, that the optimal method for keeping the horse’s brain actively involved in any learning or memorisation task is to provide variation in the animal’s envi- 5 ronment and activities. There is certainly anecdotal evidence to suggest that horses require active learning behaviours to maximise learning potential and memorisation and that horses only learn and remember very poorly under passive conditions (the acquisition of learning without the motivation to do so). This is an area, which requires further objective assessment in terms of memory limitations and the implications this has for contemporary training schemes. Objective measurement of memory capability in the horse, and, comparisons of performance of learning and remembering under both active and passive systems, would provide useful data in terms of equine learning and behavioural processes. 5. Experimental task learning and behaviour in the horse Some of the earliest experimental work designed to investigate equine learning demonstrated that horses could discriminate between a regular feed box and a feed box that was covered with a black cloth (Fig. 1), and younger horses exhibited fewer fear responses and more interest in new stimuli (Gardner, 1937a). This result has potential implications for contemporary training schemes suggesting the possibility of identifying a most advantageous time for learning in the horse. Such a clearer understanding of, and at what point in terms of age or perhaps neural and behavioural development, horses learn optimally would also have welfare implications for dealing with equines. Further evidence of differences in age related learning followed during a subsequent study using 62 equine subjects, where the cloth was alternately placed either above or below the feed box (Gardner, 1937b). In this second study the number of errors made by the horses increased. It should be remembered however, that there is an adaptive value for the horse in perceiving and responding, usually by avoidance, to small changes in a familiar environment. The second study also indicated that although the learning curve for all horses showed a rapid initial descent, the younger horses still learned the correct behaviour more readily than older horses, even though the differences were not significant (Gardner, 1937b). While no sex differences in learning behaviour were actually reported during the Gardner studies, in total contrast to the female horses, 32 of the 37 male horses removed the black cloth from the feed boxes during the trials to access the feed boxes Fig. 1. An artist’s impression of the Gardner feed box. From one of the earliest experimental trials for horses (from Gardner, 1937a,b). 6 J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 (Gardner, 1937a,b). The placement of the black cloths in different locations added to the difficulty of the task and perhaps challenged the spatial awareness of the horses. In an experimental study of 62 horses’ aptitude for discrimination processes and learning behaviour, Murphy et al. (2004) reported sex differences in learning skills and visuo-spatial ability in the horse. The findings indicated that male horses appeared to have benefited from superior visuo-spatial ability, as has also been reported in other species including humans (Masters and Sanders, 1993), meadow voles (Kavaliers et al., 1998) and rodents (Roof and Stein, 1999). There may be subtle sex differences in elements of learning behaviour or perceptual ability in all species and how such a phenomenon affects the horse could have implications within equitation and the contemporary training environment. 5.1. Experimental testing of equine learning and behaviour Reversal learning is the ability to adjust responses when the reinforcement values of stimuli are changed. As an experimental technique, reversal learning has also received some attention in equine behavioural studies. Where horses were required to discriminate between a black feed box and a white feed box, the horses were not only successful in the discrimination task but they were also successful in learning a daily reversal as to which box contained the feed (Warren and Warren, 1962). Experimental designs have also simultaneously encompassed both visual reversal discrimination (different colour feed buckets) and spatial reversal trials (left or right positional placement of the target feed bucket) in the horse. In general, findings from such studies have demonstrated that horses were successful in learning both types of discriminations, but that the spatial reversals were more easily learned than the visual reversal problems. There are however, conflicting reports of exactly what colours, degree of luminescence and perhaps shades of colour horses can successfully learn to discriminate (Macuda and Timney, 1999; Smith and Goldman, 1999; Saslow, 1999; Geisbauer et al., 2004; Hall and Cassaday, 2006). It may be that the location of the food source or other stimulus is a more salient cue than colour cues, particularly within reversal trial designs. For example, Mal et al. (1993) reported that foals generalised the location of food after only one trial within a 40 compartment apparatus. Interestingly however, foals appeared to have very short attention spans in that they exhibited almost total extinction of the desired response within 2–3 min of the commencement of the experimental condition. However, Mal et al. (1993) concluded that a one-trial appetitive conditioning protocol may have useful application for learning research in the horse. 5.2. Horses experience learning difficulties due to temporal delays Food reinforcement is widely used as a positive stimulus in equine learning and behavioural experimental trials, although freedom from aversive stimuli has been adjudged as more reinforcing than food provision in the horse (McGreevy, 2004). Studies of equine pattern discrimination (using a food reinforcer) have shown that horses successfully selected the correct choice option of pairs of simultaneously presented cue cards (McCall, 1990). However the introduction of a temporal delay (of only 10 s) into experimental trials, where horses were attempting to access the correct option of two spatially diverse feed buckets, following provision of the eliciting stimulus appears to cause a significant degree of difficulty for the horse (McLean, 2004a). This level of learning would appear to demand proficiency on the part of the horse at level 5 or even level 6 from the Hierarchies of Learning Skills as listed in Table 1. Why the horse should experience difficulties with temporal delays of such small magnitude is certainly interesting if not totally understood, and poses a significant challenge to designing training programmes for the horse. Perhaps motivational issues, attention behaviour, memory shortcomings or the inability to ‘chain’ or interpret on the part of the horse are critical factors influencing temporal delay based experimental trials. Several species of birds, primate and dolphins apparently demonstrate the capacity to deal with temporal delay trials, at least, under some experimental conditions and pigeons in particular have demonstrated this ability (Hope and Santi, 2004). Goats have been trained successfully to discriminate visual stimuli in delayed response tasks (Soltysik and Baldwin, 1972; Baldwin, 1979). It is unclear whether learning difficulties under such conditions challenge memory or intelligence status or both in the horse. Perhaps efficient learning of this nature requires an element of ‘un-learning’ of a previous episode before the new learning behaviour will become effective in the horse. Sappington et al. (1997) have suggested that horses may have difficulty in replacing ‘old learning’ with ‘new learning’ and this might account for lack of progress in some experimental studies and training regimes. In this regard, it may well be that the law of primacy (first learned is best learned) is far more critical to equine training programmes than was originally acknowledged (Atkinson and Shiffrin, 1971). If the law of primacy influences learning behaviour in the horse to the extent of causing difficulties with re-learning, this may have major implications for equine training programmes. 5.3. Maze learning trials in the horse Various types of maze, often with more than two choice options, have been employed to investigate learning behaviour in several rodent species. The maze method has also been utilised with larger animals including sheep (Liddell, 1925), pigs (Koba and Tanida, 2001), cattle (Arave et al., 1992) and horses (Kratzer et al., 1977; Haag et al., 1980). McCall et al. (1981) conducted exploratory research using a Hebb–Williams closed maze field to investigate the extent and degree of equine maze learning abilities. The horses were presented with a different maze problem every day for 12 days. The findings indicated that the horses were capable of learning the new maze problems. This approach also permitted the researchers to apply a rating of the horses’ learning ability by ranking the horses based on the order and magnitude of their maze learning ability under test conditions. It would be interesting to re-visit this area of equine research and examine the repeatability of the rankings assigned to individual horses J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 and to assess performance based on rankings across a range of different maze problems. The use of maze testing in equine memory and learning behaviour has also been reported as having had important beneficial results. In one study, the authors declared that the horses were found to not only learn and understand the problem, which was presented, but Marinier and Alexander (1994) also concluded that the horses understood the principles behind the problem. However, it appears that there is still little evidence suggesting a correlation between rankings on different types of experimental trials in the horse. This may be purely a reflection of the horses’ ability or inability to perform under certain conditions or equally perhaps, inappropriate experimental trial design on the part of researchers. Nonetheless, it would appear that some horses are better at learning certain individual and specific tasks, while other horses perform better at different tasks. In particular, a lack of correlation in the findings for the same horses between the outcomes of spatial (following a route) and instrumental (opening a wooden box for food) tasks would seem to suggest that both tasks might actually require different learning processes and ability in the horse (Wolff and Hausberger, 1996). 5.4. Sidedness could influence learning and behaviour in the horse There is increased interest in the topic of sidedness or laterality among ethologists and evolutionary biologists (Ventolini et al., 2005). While the study of laterality was originally more associated with neurology and neuropsychology, it has become apparent that this phenomenon is not just unique to man but widespread among other species also (Vallortigara et al., 1999). Sidedness or lateralised motor behaviour in the horse may have the potential to influence maze-testing outcomes and laterality has been shown to convey a negative influence on athletic performance in the horse (Dalin et al., 1985). When designing experimental trials involving maze or choice tests for horses, care should be taken to consider the possibility of inherent sidedness associated with the subjects. Previous experimental choice trials in cattle have shown that cattle were reluctant to change from one side of a maze apparatus to the other (Grandin et al., 1994). More recent work in dairy heifers has shown that the animals learned to choose a preferential side of a Y maze in an attempt to avoid an aversive stimulus such as noise (Arnold et al., 2004). Kratzer et al. (1977) set out to measure the learning ability of horses in a situation relatively free of human interactions during testing where the animals had to choose a correct escape route. The authors had assumed that learning would have been reflected in the simple maze by a decrease in the number of errors, a decrease in latency of escape and the tendency to choose the correct escape route. The results from this study showed that preferences for left and right choices varied among the horses, and, curiously, taller and thinner horses tended to opt for the left choice alternative. As is the case, in many species, male horses tend to be taller than their female counterparts and the results may have been due to a sex affect. On the other hand, it 7 may have occurred due to breed differences in reactivity such as those reported in many recent temperament and personality trials (Le Scolan et al., 1997; Momozawa et al., 2003). Nonetheless, in other studies, individual sidedness choices of horses have revealed patterns significantly different from random choice expectations where individual animals exhibited pronounced laterality. Grzimek (1968) reported observations of 53 horses in which 77% of horses observed displayed a preference for the foot used to paw, 67% had a preference for a foot to initiate walk and 23% of the horses had a foot preference for galloping, and therefore indicated significant degrees of sidedness in the test subjects. Although significant right handed bias has been reported in humans (Rife, 1940; McManus, 1985; Klar, 1996; Annett, 2003) there is a higher incidence of left-sidedness observed in human males compared to human females (Gladue and Bailey, 1995). Similar trends have been reported in rodents (Waters and Denenberg, 1994), domestic dogs (Wells, 2003) and more recently in the horse (Murphy et al., 2005; McGreevy and Rogers, 2005). As a consequence, experimental trials involving food preference choices in the horse could be influenced by sidedness issues and it would be important to control for sidedness when conducting this type of experimental work in equine diet preference type trials. McGreevy and Rogers (2005) have highlighted that the convention of handling horses from the left side could possibly influence side bias with regard to motor behaviour even when the horses were not being handled. Studies of feral, unhandled or young naı̈ve horses (foals) may provide more accurate data outlining the extent and impact of laterality in the horse. 6. Social and observational learning True observational learning is a complex higher mental ability predicated on reasoning and insight to allow exact imitation (Nicol, 1996). Horse handlers have regularly trained younger animals to follow older more experienced horses over jumping obstacles, to travel together in transporters and stand at ease beside conspecifics for procedures such as clipping and shoeing. Whether or not this constitutes absolutely true observational learning, it is generally accepted that young/naı̈ve horse learn something at least from older/more experienced conspecifics (Kiley-Worthington, 1987). There are some reports albeit anecdotal, suggesting that horses may develop undesirable stereotypic behaviours as a direct result of observational learning (Kiley-Worthington, 1983; McGreevy et al., 1995) but the majority of scientific data to date does not appear to support this thesis (Cooper and Nicol, 1994). It does seem however, that at least some animals actively learn to imitate stereotypic behaviour by observing conspecifics and voles exposed to such activity have acquired the learned behaviour earlier and perform the stereotypic behaviour for much longer periods (Cooper and Nicol, 1994). Nicol (1995) reviewed studies on the ability of a number of species of domestic animals to acquire information and skills by observation of conspecifics. There was some evidence of varying levels of social learning in pigs, hens, dogs and cats. Hens and cats demon- 8 J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 strated impressive social learning skills; pigs and dogs to a lesser degree, while both cattle and horses performed less well in this regard. No significant evidence of true observational learning has, as of yet, been produced in the horse following several studies (Baer et al., 1983; Baker and Crawford, 1986; Clarke et al., 1996; Lindberg et al., 1999). However, this lack of enhanced social learning reported in the horse may be an artefact of the experimental conditions and trial designs employed with equine subjects to date. Further work in this area is warranted as it does seem likely that there could be some real advantage associated with enhanced social learning skills (if indeed it exists) in the horse. It may be that actually designing an appropriate experimental set of conditions to investigate social and observational learning in the horse is a more complex task than has been originally thought. More recent attempts have been made to address this issue but the methodology although modified somewhat was basically similar to that employed in earlier work (McLean, 2004b). Clarke et al. (1996) revisited the issue of observational learning in horses and broadly based their study on the earlier methods used by Baer et al. (1983) with some adjustments. They tested fourteen horses of mixed age and breed (seven controls and seven observers) where the observers were exposed to correct performances of a trained demonstrator (an unfamiliar horse) for 20 trials over 2 days. The controls, although handled and subjected to the similar placement procedures, were not exposed to the demonstrator conducting the task. As had been the case with the earlier (Baer et al., 1983) work, Clarke et al. (1996) found no significant effects of prior observation on discrimination accuracy in the feed related task in the horses. There were however, strong significant effects of prior observation on latency to approach the goal area on the first trial. Might there be scope to develop training based on ‘chaining processes’ whereby the horse might learn some desired behaviour if this latency to approach the target area were harnessed? It would seem that the horses were at least better motivated to participate immediately following exposure to the demonstrator. One other point worthy of note in the Clarke et al. (1996) study was the fact that the demonstrator was an animal not known to or familiar with the test subjects prior to the experimental conditions. The familiarisation protocol only required that the demonstrator be stabled ‘next door’ for a period of 18 h for social customisation. Was this sufficient time and did the conditions imposed allow for adequate socialisation among the horses, or could this mechanically controlled social contact have had any adverse affect on the learning outcomes of the experimental animals? Perhaps observational learning may be influenced by a dominance or alpha type factor whereby subjects might have more interest in or possibly be more motivated by the actions of a ‘respected’ conspecific. It may be important to employ a dominant type animal as the use of the acknowledged alpha leader of a group of test subjects might be more influential in terms of interest and attention on the part of the test subjects. Whatever the case may be, it appears that horses pastured outdoors in small groups learn to complete trials and training programmes more quickly than horses housed singly in stalls (Rivera et al., 2002; Sondergaard and Ladewig, 2004). It has also been proposed that horses kept in group situations realise their motivation for social behaviour more easily and, as a consequence, such interaction allows the horses to understand the signals better from a trainer or handler (Sondergaard and Ladewig, 2004). Certainly, issues such as motivation and attention would appear to be a very important concern for consideration in such circumstances. A better understanding is required of how these qualities impact on the behavioural and learning processes in the horse. 7. Attempts at assessing higher order cognition in horses Intrinsic conceptualisation capability or the ability to form concepts based on some common characteristic among different stimuli involves greater mental ability and higher cognitive function on the part of an organism or species (Table 1). There had been no known research prior to 1994 detailing investigation of concept learning in horses. Sappington and Goldman (1994) designed a study to test the ability of horses to perform at this level of the hierarchy of learning skills as per Thomas (1986). Perhaps one problem with attempting to assess concepts theory in another species is that humans have previously decided what the common characteristics between stimuli actually are. However, as we often realise to our peril, even between humans, perceptions can and do vary enormously, with different individuals often deducing a different meaning or concept from identical stimuli. Sappington and Goldman (1994) presented a series of two choice discrimination problems on stimulus panels that could open to allow access to food bowls in an attempt to explore concept formation ability in the horse. The results demonstrated complex pattern discrimination ability in horses, and suggested that they may be able to solve higher order problems using concept formation in some problem solving scenarios, which equates to at least level 6 as per Thomas (1986). The conceptually based discrimination task such as that used in the Sappington and Goldman (1994) study is a much more challenging problem than a simple discrimination task for any species including the horse. This is because it requires that the subjects recognise or perhaps more accurately realise and understand that different stimuli share a common characteristic and the characteristic is in essence the focus of the desired goal directed behaviour. There have been more recent attempts to assess higher order cognitive ability in the horse. In the standard identity matchingto-sample format (IDMS), experimental subjects are presented with different coloured lights, shapes, sounds, or static versus moving stimuli. Initially a sample stimulus is presented in the centre of a stimulus array and response to the stimulus by the subject prompts the presentation of two comparison stimuli. One of these stimuli is physically identical to the sample and the second acts as a distraction. The subject is rewarded when responding to the comparison stimulus that is the same as the original sample stimulus. Flannery (1997) used a similar conceptually based or conditional discrimination procedure (an adaptation of an IDMS task) to test if the subjects realised that there was a relationship between stimuli. That study used cards on a wall background to test the acquisition of relational discrimination ability in the horse. The results of the study demonstrated that: J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 (a) horses could discriminate matching shapes; (b) the ability to discriminate was not adversely affected by an intermittent primary reinforcer; (c) altering the manner in which the stimuli are presented (on a novel background with greater distance between stimuli) did not produce a significant decrement in accuracy. Flannery (1997) concluded that the performances throughout this study showed the ability of horses to engage in higherorder discriminations, and that horses successfully learned the relational discriminations and demonstrated their ability to generalise this learning under several different conditions. There have been reports of further work, which provides compelling evidence of horses with the ability to demonstrate conceptualisation under experimental conditions. Horses have successfully participated in experimental trials, which have specifically investigated the study of relative size among objects and the use of two and three-dimensional objects with open or closed centres (Hanggi, 1999, 2003). Concept formation, based on the criterion of differentiating between hard and soft materials, has also been successfully demonstrated where ponies acted as the experimental group (Watt and McDonnell, 2001). How learning or perhaps degrees of learning ability is likely to influence participation in future training is an important issue when dealing with the horse and this has considerable implications for training. The relationship between learning ability and training ability has been addressed in a number of equine studies. Fiske and Potter (1979) reported a positive correlation between the test performance of young horses on a serial reversal learning task and subsequent training for riding. On the other hand Marinier and Alexander (1994) failed to find any positive correlation between handling or training behaviour and learning ability during a maze test. However, positive correlations between ratings of learning ability and individual behavioural reactions of the horses during experimental trials at several different riding schools have been reported (Le Scolan et al., 1997). There is an obvious difficulty in this type of study, whereby factoring in the influence of different handlers is at best almost impossible and needs much attention in future investigations. 8. Learning and behaviour in the feral horse Feralisation has been described as the opposite or the reverse of domestication and therefore the feralisation process per se cannot occur in individuals, rather it is restricted to populations of animals (Daniels and Bekoff, 1989). Previous studies have reported that free-ranging or feral horses have learned to occupy a home range and generally will attempt to return to this broadly defined area of the home range following relocation through human interference (Goodwin, 2002). Behavioural studies of feral populations of breeding mares have provided some interesting findings whereby after foaling, mares with foals were reported to have separated off into distinct subgroups (van Dierendonck et al., 2004) It appears that feral mares attempt to keep the foals at a safe distance and separated from the more energetic geldings and sub-adults in the feral population. What is not absolutely clear however is if this behavioural activity is totally at the behest of the mares or if it also results at least to 9 some degree from increased mutual attraction between the foals. The remaining barren or control mares within a herd situation actually tend to increase interaction with the rest of the herd. Klingel (1975) proposed a bonding theory whereby pregnant mares separated themselves from other members of the herd for a period of several to many hours prior to and around time of parturition. It seems logical that this behaviour is important in allowing the neonatal foal sufficient time to recognise, initiate the bonding process and/or perhaps ‘imprint’ on the dam. In both feral and domestic populations of horses, foals are precocious developers and, unlike calves or fawns, which tend to lie in undergrowth, can gallop with their dams within a few hours of birth (Goodwin, 2002). Foals generally ‘learn’ to stay within the immediate proximity of the dam during the first weeks post-partum and begin to engage in exploratory trips away from the dam with other foals between one and two months of age. While foals bond to and appear to learn from their dams, they also learn to recognise individuals within their own species. Although the likelihood is that there is a natural instinct present to do so, the foal also appears to learn about feeding and ingestive behaviour and perhaps sheltering behaviour by participation with and imitation of its mother in early life. Learning behaviour in the foal results from developing and practising locomotory skills and other playing behaviours between foals at this early stage (Carson and Wood-Gush, 1983; 1996). The play activity is seen as critically important in order that foals learn to interact with one another and equally in the social establishment of pair bonds (McGreevy, 2004). Perhaps interestingly, in terms of the mare-foal dyad, Houpt et al. (1982) concluded that dams did not appear to teach their foals with regard to learning a spatial task. However others have suggested that there may be a genetic influence whereby the ability to deal with spatial tasks in the horse is more likely to be inherited from the sire (Wolff and Hausberger, 1996). Studies of equine reproductive behaviours in feral horses might be useful when designing training programmes that propose to optimise learning in the horse. Some findings to date indicate that in feral or free-ranging situations, younger colts appear to learn something of sexual behaviours from observations of the stallion copulating with the harem mares—the so called Fraser Darling effect (Wilson, 1975). It also appears that reproductive success is much enhanced by the development of stable relationships between mares and a single stallion in free-ranging groups and such activity also has the effect of reducing aggression between the individual animals (Linklater et al., 1999). Furthermore it seems likely that all horses are capable of easily learning (understanding) the hierarchical ranking system in a group or herd, whether it be linear or even more complex (Houpt et al., 1978). There is still much to be gained from observations of feral horses and their environmental interactions with regard to behavioural ecology and learning processes, which will lead to greater understanding of the equine cognitive processes from the human point of view. In this vein, Houpt and OgilvieGraham (2004) have recently stressed the importance of the providing appropriate conditions for the domestic horse based on the range of behavioural and learning activity demonstrated in feral or free-ranging equine groups. 10 J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 9. Contemporary training schemes and equine learning Modern companion and performance horses are increasingly required to perform tasks unlikely to emanate from or indeed be represented in the natural or feral situation. Some of the current competition and equine husbandry systems present conditions where horses have to deal with unnatural obstacles and other features that feral horses would naturally or could otherwise avoid. This contrasts with evolutionary adaptive behaviour for horses, e.g. jumping, negotiating or manoeuvring around simple or more elaborate series of impediments or negotiating entry into dark or narrow areas such as stocks, starting stalls or trailers. Several of these tasks require the horse to suppress many of its natural instincts and also either to have or acquire the ability to discriminate and respond to a wide variety of different stimuli (McCall, 1990). Many learning and behaviour studies have routinely challenged the horse to perform trials in a context not particularly common in practical horse training (Sondergaard and Ladewig, 2004). However, the ability to learn and perform or respond to the different stimuli influences not only the economic value but also the status (intellect) of the individual horse to an owner or trainer. Curiously within the disciplines of equitation, learning of the desired behavioural processes is most often attempted using negative reinforcement strategies (McCall, 1989). Negative reinforcement strategies are premised on the removal of a stimulus (typically an aversive stimulus) to obtain the desired behaviour (Chance, 1993). Yet on the other hand experimental designs to actually measure, assess or induce learning and desired responses in the horse rely almost exclusively on primary positive reinforcement regimes (Nicol, 2002). In contrast, the basis for positive reinforcement is the addition of a desirable stimulus following exhibition of a desirable behaviour (McLean, 2004b). Furthermore, horse trainers are isolated from advances in animal training and are largely unaware that they are using negative reinforcement in training (McLean, 2004a). Contemporary training schemes and the innate intelligence of the horse might be more harmoniously employed following clearer definition and better usage of the intrinsic behavioural and learning processes in the horse. 10. Cellular and molecular basis of equine learning behaviour While interest in equine learning, behaviour and welfare issues is growing, much more research in these areas needs to be undertaken so as to continue to improve our understanding of equine ethology and ultimately benefit the horse-human relationship. As the status and value of the horse continues to appreciate in terms of a companion animal, investigating issues such as natural balance, sidedness and idiosyncratic biomechanical gait preferences in performance horses is likely to yield useful data with regard to improving performance and contemporary training schemes. Motor laterality has been previously studied as an indicator of cerebral hemispheric asymmetry and various learning abilities have been associated with the different sides or cerebral structures of the human brain (Coren, 1992; Hellige, 1993). Ventolini et al. (2005) have highlighted the fact that there is a growing understanding that laterality affects subjects, particularly animals with laterally placed eyes, not only under controlled experimental conditions but in more natural conditions also. The use of magnetic resonance imaging (MRI) and positron emission tomography (PET) scanning techniques have greatly advanced the understanding of brain activity in terms of learning behaviour in humans. The development of appropriate experimental trials is complicated by particular logistical and management difficulties for this technology in dealing with other species like the horse. But this technology may prove both very applicable and useful in the future and provide hitherto unavailable data regarding learning and behaviour in the horse. There has been remarkable progress in terms of molecular and cellular approaches to biology and the workings of the nervous systems are now being unravelled by the neurosciences. It may soon be possible to have a clearer understanding of a range of different equine behaviours in terms of the underlying processes and mechanisms. Investigative laboratory techniques including neuronal histology (albeit post mortem) of the pre-frontal and parietal cortex and other brain structures may yet yield further fascinating insights into equine behaviour and learning processes. Comparative investigations between feral or free-ranging and domestic horses, in the areas of spatio-temporal behavioural patterns of male and female foals prior to weaning, and the effects of stress on the mental processes in young horses, may elucidate more fully, the learning, attention and motivational attributes of the horse. Investigations of equine visual systems, perceptual ability and particularly attention studies may have much more to yield. Male and female monkeys have been reported to select different human targets as the focus of their aggression and possibly view humans as agonistic competitors (Hosey, 2005) and similar studies in the horse might prove equally enlightening. Technological advances have made enormous strides in terms of understanding human behavioural and learning processes based on neurobiological and psychological assessment from MRI and PET techniques. Detailed investigations of the equine visual system in the form of eye-tracking studies might yet provide useful data to aid our understanding of the extent of perceptual abilities and the link between training and learning ability in the horse. Research of this nature, as soon as it is feasible, would do much to enhance the understanding of the behavioural and learning processes in the horse. Acknowledgement The authors would like to thank Debbie Goodwin for advice and helpful suggestions. References Annett, M., 2003. Cerebral asymmetry in twins: predictions of the right shift theory. Neuropsychologia 41, 469–479. J. Murphy, S. Arkins / Behavioural Processes 76 (2007) 1–13 Arave, C.W., Lamb, R.C., Arambel, M.J., Purcell, D., Walters, J.L., 1992. 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