Lateralised Behavioural Responses in Livestock to Environmental Stressors: Comparison
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Lateralised behavioural responses to environmental stressors have become more frequently used as indicators of social welfare in animals. These lateralised behavioural responses are under the control of asymmetrical brain functions as part of the primary functions of most vertebrates and assist in primary social and survival functions. Lateralised behavioural responses originating from the left hemisphere are responsible for processing familiar conditions, while the right hemisphere is responsible for responding to novel stimuli in the environment. The forced lateralisation and side preference tests have been used to determine the visual lateralised behavioural responses in livestock to environmental stressors. Limb preference during movement has also been used to determine motor lateralisation. 

  • lateralisation
  • infrared thermography
  • behavioural responses
  • stressors
  • livestock
  • welfare conditions

1. Introduction

The assessment of the cognitive, mental, and emotional welfare of animals is increasing in importance [1[1][2][3][4][5],2,3,4,5], as formal welfare assessments are mainly based on animals’ health [6,7][6][7]. In addition to traditional assessment strategies, several studies have given particular attention to the validation of lateralised behaviours as being welfare indicators of the animals’ cognitive and emotional welfare. For example, Knierim et al. [8] stated that behavioural responses that are related to high proportions of fluctuating cerebral asymmetry could indicate poor welfare. Therefore, understanding the process of the lateralised behavioural visuospatial responses to a challenging environment could help to avoid the suffering and distress of animals [9,10,11][9][10][11].
Lateralisation means asymmetry of body functions [12], which enhances neural processing through the reduction of conflict and interference that improves task performance [13]. Examples of these are the left- and right-handedness in humans and limb preferences in animals [14,15,16][14][15][16]. The fundamental and complementary patterns of brain hemispheric lateralisation in vertebrates include the involvement of the right hemisphere in rapid responses and the left hemisphere in the control of motor responses that require some degree of initial inhibition before a final decision is made. For example, the preference of using the right forelimb (i.e., left hemisphere) by vertebrates when fine motor manipulation is required to be performed [17].
Environmental stimulation has an important role in the development of brain lateralisation [18]. The exposure of animals to environmental stimulation in their early life enhances brain lateralisation that could prepare them to live in a world that requires good cognitive ability. For example, Lyons et al. [19] found that intermittent separations of Saimiri monkeys from their mothers led to more stimulation, which, in turn, leads to the development of a lateralised brain. Conversely, lower environmental stimulation links to less variable brain function and redundancy (symmetrical/non lateralised) and thus fewer demands on the animal’s cognitive ability. For example, light deprivation during early stages of chick development has shown to impede the development of brain lateralisation. Hens normally block light from reaching the eggs during incubation but occasionally leave their nest, exposing eggs to light for short durations, which then leads to brain lateralisation in the developing chick. Light deprivation in chicks at this early developmental stage could potentially indicate a poor living environment, which would then lead to brain redundancy [18].
Lateralisation of behavioural responses and the connection with brain laterality has been studied in a variety of species, specifically where the lateralisation is associated with stress [20,21][20][21]. Stress comes in two forms: acute and chronic. Acute stress stimulates the hypothalamus to secrete more vasopressin than corticotropin-releasing hormone, whereas chronic stress has the reverse effect and is often associated with prolonged high levels of cortisol. Animals’ ability to run or fight is elevated when growth hormones and blood sugar levels are affected, which enables them to react to acute stimuli quickly. Chronic stress, on the other hand, leads to long-term consequences, like stunted growth and heightened illness vulnerability [22]. This chronic stress (and corresponding prolonged high levels of cortisol) influences the lateralisation of behaviours and can therefore become an indicator of welfare for animals. For example, intensively housed cattle, who are reared almost entirely indoors (with limited pasture access), showed more lateralised responses than those with continuous access to pasture (with indoor housing at night) [23]. Stub et al. [24] reported increased evidence of lateralised leg use in rats housed individually on a grid floor when compared to those housed socially on bedding. Moreover, Tuyttens et al. [25] found that rabbits housed in enriched and low-density cages exhibited fewer lateralised responses than those housed in barren and high-density cages.
Furthermore, studies have shown that lateralised behavioural responses reflect how animals overcome specific emotional conditions, facilitating the classification of emotions via valence and arousal [26,27][26][27]. These can be studied by blocking the sensory organs in the left side and subsequently the right side and comparing the differences in lateralised behavioural responses [28]. These have also been studied using specialised tests like the detour test for visual responses [29], the head-turn test for auditory responses [30], and the orienting asymmetry paradigm [31].
The role of lateralisation has also been studied with regards to stress and social interactions within the domestic environment. The evolution of social behaviours is related to the development of higher cognitive abilities [32] and the ability of individuals to distinguish between conspecifics. For example, researchers have found that Bos taurus cattle could distinguish between conspecifics in addition to specific visual discrimination [33]. In the same context, Vallortigara and Rogers [13] found that social interactions were also lateralised within species. This specialised lateralisation helps an individual to avoid being attacked by another through approaching the latter on its right side, thus avoiding its antagonistic left side (i.e., right hemisphere). Therefore, social recognition was found to be processed in a consistent pattern in vertebrates, with the right hemisphere responsible for individual recognition and the left hemisphere responsible for distinctions between conspecifics and heterospecifics [34].

2. Relationships between Sensory Lateralisation and Behavioural Responses

Animals’ behavioural responses are dependent upon how they perceive and understand their environment [66][35]. As part of their learning, sensory cues are processed as either positive or negative stimuli, which assist animals in seeking or avoiding pleasant or unpleasant environmental consequences [67,68][36][37]. For example, dairy cows learn to enter a milking parlour by associating auditory cues with food rewards [69][38]. Also, domestic ungulates use their sensory cues to discriminate between ‘friends and foes’ and, accordingly, decrease or increase their level of vigilance [70][39]. For example, cows decreased their vigilance and increased foraging rates for the high-quality forages when they detected olfactory or visual cues from a heterospecific species placed near the high-quality food. The opposite responses occurred when a predator species was placed near the high-quality food [70][39]. Sensory lateralisation is a subfield of lateralisation in which the expression of lateralisation in the visual, olfactory, and auditory senses changes in mammals and humans during particular situations. These are controlled via hemispheric specialisation, as mentioned above. Rogers [64][40] proposed that the preferences of the use of a specific eye, ear, and nostril can help in understanding cognitive processes. Also, identification of the particular eye, ear, and nostril involved in the response can represent how the animal is processing its environmental stimuli. This lateralised preference also indicates an effect on emotional responses [71][41].

2.1. Visual Lateralisation

Domestic livestock ungulates have specific visual fields related to the placement of their eyes (on the sides of their heads) that affect their behaviours with regards to how they orientate themselves to stimuli. Knowledge regarding these animals’ visual fields of view can therefore provide additional information to the importance of visual lateralisation and behavioural responses to environmental changes. For example, cows depend on vision for about 50% of their information. Their eyes are located on the sides of their head, so they have a wide field of view (about 330 degrees). However, they have a limited binocular field of vision about 30–50 degrees, with a blind spot directly behind them [72][42]. Like cattle, horses have eyes on the sides of their heads and are able to detect and discriminate between stimuli in an almost full 360-degree circle around them, including a panoramic field of view [73][43]. Vertebrates and non-vertebrate mammals have little or no overlapping of the visual fields of view (sided eyes). This means that these types of mammals process their visual information in a lateralised way [74,75][44][45]. These mammals employ lateralised behavioural patterns to assess their surroundings by adjusting their head position and using eye movements to indicate lateralisation [29]. The fundamental process of the lateralised vision therefore depends on the connection of the left field of vision to the right brain hemisphere and vice versa. These perceptual asymmetries have been observed and measured in daily management routines. In their daily lives, animals must make choices regarding their daily routines, providing researchers some insight into their stress and emotional responses based on the lateralisation of behaviours during these decision-making processes. Fraser and Matthews [76][46] reported that such preferences aid in assessing what could be important for animals, thus improving their welfare. For example, horses displayed right side visual preference for novel objects (neutral emotional valence), left eye preference for objects with negative valence, and no side preference for objects with positive valence (suggesting binocular vision was used) [71][41]. Furthermore, under new environments, horses often use the left eye to assess conditions, especially when a human is present, and also showed left eye preference when assessing or scanning a novel human [77][47]. Since horses are traditionally trained to accept humans on the left side, horses in this particular study were trained to accept a person on both eyes to alleviate side bias [77][47].

2.2. Auditory Lateralisation

Much like visual lateralisation, auditory lateralisation is also important in assessing welfare and analysing behavioural responses in animals. Auditory senses are much more sensitive in cattle in comparison to humans. Cattle perceive a wider range of frequencies (from 23 to 37,000 Hz), with a maximum sensitivity of 8000 Hz [78][48]. These hearing frequencies enable them to detect predators at greater distances and to locate the source of noises [79][49]. This trait also enables them to hear and identify their own kind. For example, a calf can recognise its mother’s calls and differentiate them from others [78][48]. Furthermore, cattle move their ears upwards to listen carefully and constantly while remaining vigilant, then localise the noise source via the auricle (external ear). This ability is effective when the noise comes from the front of the animal, but it is reduced to 25° if the noise is at the sides of the animals’ heads [80][50]. Therefore, cattle must turn their heads to identify the noise source. Andrew [81][51] reported that the head and ear orientations in mammals, called the “orientation reflex”, are considered an external clue for the arousal state of the animal. In this sense, the arousal state can be determined by observing changes in head orientation of the passive unrestrained individuals in response to the playback of vocalisation of familiar conspecifics from behind. These changes in orientation have also been used for examining lateralised responses to acoustic stimuli in mammals tested under unrestrained contexts [82][52]. The direction of the head turning indicates the role of the contralateral hemisphere in the acoustic stimulus processing. For example, an individual turns its head while the right ear is directed towards the speaker to process inputs from the right ear via the left hemisphere [82,83][52][53]. Although the turning of the head in many species does not allow the observer to distinguish between visual and auditory lateralisation, this can still be determined by retraining the head and only allowing the ears to move in response to sound [84][54]. Under these circumstances, individual animals can direct their ears and/or head either independently or simultaneously towards the sound source and demonstrate laterality and neurological processing. Auditory lateralisation has been studied in a variety of species in which the hemispheric specialisation is affected by various factors, such as sound structure, species, and type of stimulus [85][55]. However, researchers have also found a large degree of duplication in hemispheric function in mammals during experiments with auditory stimuli, where each ear connects to both brain sides due to varies decussations and commissures beginning in the medulla [86][56]. In this case, each hemisphere receives signals from both ears, and then processes them and makes comparisons between the right and left ear inputs without the intervention of the other hemisphere. During this processing, one hemisphere could localise sound at any point in the horizontal plane or decode speech/sound entering either ear, even in the absence of cerebral commissures [87][57]. Therefore, the auditory signal can be processed predominantly in the contralateral hemisphere, leading to asymmetrical processing even if one ear is connected to both hemispheres [88][58]. Thus, if researchers observe an animal turn its head to the left or move the left ear backwards towards the sound, this indicates control via the right hemisphere and vice versa [83][53]. This is consistent with findings that the vocalisations of conspecifics were reported to be processed within the left hemisphere [89][59]. In other studies, cattle’s sense of hearing was reported to determine its behaviour on the farm as they adapted to familiar noises. This is true even for novel, intense, or high-pitched sounds that may lead to fearful reactions [90][60]. However, this is not the same for low-pitched sounds, which tend to soothe the animal [90][60]. In addition, voice inflections in people and the degree of familiarity of the voice can lead to behavioural changes [91][61]. For example, the sound of a human cry (scream) can lead to more expressed agitation in cattle than a metallic sound. Moreover, Waiblinger et al. [92][62] stated that cattle respond to variations in human vocalisation ranging from soothing sounds to signals indicating danger that resulted in behaviours indicating fear, aggression, or uneasiness. Furthermore, cattle seem to dislike shouting more than aversive physical contact [93][63]. A similar phenomenon has also been observed in horses. Auditory responses in horses have shown that they use the left hemisphere (right ear) to process vocalisation from horses that they recognise, but are outside of their social group, and the right hemisphere (left ear) to process vocalisation from unknown horses [85][55].

2.3. Olfactory Lateralisation

Most mammalian species can detect and discriminate different odours and pheromones through olfaction. There are differences not only between species but also individuals in their olfactory sensitivity. Most researchers studying the olfactory sensitivity in mammals depend on behavioural testing [94][64]. For example, stressed cattle, or its urine odour, can modify the behavioural reactions of its conspecifics [95][65], like slowing the learning ability in heifers [96][66]. Moreover, a longer latency to start feeding in addition to a slower feeding rate were observed in cattle approaching an object contaminated with the urine of stressed conspecifics. This indicates increased fearfulness, which is mediated through olfactory signals from the pheromones in the urine of distressed animals [95][65]. Therefore, pheromones can be considered as an alarm signal to herd members. In addition to non-human animals, olfactory responses were also reported to be lateralised in humans [97][67], in which the right nostril (i.e., right hemisphere) was found to respond to unfamiliar odours [98][68]. However, in another study by Broman et al. [99][69], it was reported that the right nostril also responded more strongly than the left nostril to familiar odours. However, in mammals, an ipsilateral ascent to the olfactory system due to the information’s transmit from each nostril to the olfactory cortex via the olfactory bulb of the corresponding hemisphere was reported [100][70]. Previous studies have deducted the lateralised processing of odour analysis in both vertebrate and invertebrate species [71[41][70][71][72][73],100,101,102,103], and it was reported that the response to novel information was under the right hemispheric control, while the left hemisphere controlled familiar information [74,101,104,105,106][44][71][74][75][76]. Therefore, the response of the right nostril (i.e., right hemisphere) to adrenaline was in line with the idea that the right hemisphere controls the hypothalamic–pituitary–adrenal axis, which is associated with the expression of arousal as well as negative emotions, such as aggression, escape behaviours, and fear [101][71]. Therefore, sympathetic activation was under the control of the right hemisphere, while the left hemisphere controlled the parasympathetic activity that is associated with calm responses [107][77]. However, olfactory lateralisation in horses has shown that there was a slight, but not significant, tendency to use the right nostril to investigate novel objects [71][41].

3. Relationship between Sensory Behavioural Lateralisation and Emotions

The link between emotions and behavioural lateralisation resulted in increased awareness of livestock stakeholders regarding enhanced adaptive fitness and welfare during regular handling of their animals. For example, during emotional conditions, visual lateralisation in cattle was observed by Robins and Phillips [9], in which the left/right eye was turned towards the emotional stimulus to process it in the contralateral brain hemisphere, a response that was considered a lateralisation measure. They recorded that 97 cattle used the left eye and 53 used the right eye to see the given negative emotional stimulus at the time of crossing the transect path. Therefore, the right hemisphere is related to the left eye that allows an animal to view the potential threat more easily [9]. Further, Siniscalchi et al. [108][78] revealed that visual stimuli with higher emotional valence (negative) also resulted in animals turning to the left side due to the contralateral brain structure’s activation. Additionally, in another study, Robins and Phillips [9] investigated the eye preferences of a cohort of cattle who were familiar with the stimuli. This group were then exposed to the same negative emotional stimuli as the ones previously mentioned, which resulted in a demonstration of a reversal of viewing preferences. Out of 72 cattle who crossed the transect path, 29 cattle used the left eye, but 43 cattle used the right eye to observe the stimuli. This directional shift in viewing preferences indicated experience-dependent learning or habitual effects on emotional and behavioural lateralisation, which has also been observed in other mammalian and non-mammalian animal species. Phillips et al. [10] observed that the cows that preferred to use their left eye to view dangerous situations were lower in the dominance order and had increased crush scores. In this study, they had demonstrated behaviours such as moving down the left-hand side when they became familiar with the “danger”, so they were assumed to be more anxious cows. Furthermore, Kappel et al. [109][79] investigated the relationship between preferential uses of the left or right eye and other behaviours while passing unfamiliar bilaterally placed objects while exiting the milking parlour. They reported that a higher number of cows approached the right object than the left. Cows that approached the left object (i.e., left eye/right hemisphere) exhibited hesitant behaviours, such as stopping at a distance and sniffing. Goma et al. [110][80] also reported that cows passing a person in the lane on their right side (i.e., left eye/right hemisphere) showed more anxious behaviours, such as sniffing to the ground, raised/tucked tail, higher crush score, and increased flight speed, than that of the cows passing on the left side. This is consistent with the study published by the authors of [64][40], who reported that the fight or flight response of an animal is mainly controlled via the right hemisphere of the brain. Therefore, the positive relationship between negative emotional stimulus and left eye view (i.e., right hemisphere) confirmed that the emotional stimuli processing was lateralised. Lateralisation has been tied to behavioural responses in horses as well. In a study of feral-living horses, researchers observed that horses had a left-side bias for agonistic and aggressive behaviours within their normal social groups as well as between stallions of different herds [111][81]. Horses in the same study were also observed to display left-side bias when displaying behaviours consistent with vigilance (assessing potential threat), as well as side movements of reactivity with relation to the potential threat, suggesting a preference to use the right brain hemisphere when assessing or reacting to aggression or novelty. However, these side biases did not carry over to movement [111][81]. Further studies have linked emotional valence with lateralisation in horses. In a study of young (one-year-old) domestic horses, individual horses who were approached from the left side by a novel human exhibited higher negative responses than those approached from the right. Slightly older (two-year-old) trained horses displayed no asymmetry. Since horses are often trained on their left side, and are therefore desensitised to stimuli on that side, research has suggested that the left side is more associated with negative or novel stimuli [112][82]. Furthermore, horses with low impulse control, indicating high emotional responses (high baseline faecal cortisol level), with innovative problem-solving capabilities who were considered tenacious also showed left-side laterality preference [113][83]. In another study, horses that were exposed to novel stimuli and wearing heartrate monitors displayed a greater use of their left side (right hemisphere), suggesting that the left side is important when making emotional decisions [114][84]. In yet another study, horses showed preference for using the left lateralisation for visual and olfactory information input when assessing stimuli associated with a negative emotional valence and no visible asymmetry when assessing stimuli with a positive valence [71][41]. Lateralisation also plays a role in social behaviours with favourite partners. Under normal conditions, horses demonstrate a left-side preference for affiliative behaviours and social interactions with favoured conspecifics [115][85]. During allogrooming, a social tactile interaction between two horses in which each horse simultaneously scratches the other with their teeth, horses stand next to one another facing opposite directions so that they may simultaneously favour the right or left side closest to their bonded conspecific. Recent findings have suggested that when expressing allogrooming behaviours under stressful conditions, horses do not demonstrate side preferences for this kind of social interaction [116][86], suggesting that while lateralisation plays a role in processing information, it may not play as strong a role when individuals are seeking affiliative interactions. Although horses and cattle have been shown to have a right hemisphere dominance pattern for processing novel or fear-inducing stimuli on a population level, there is no significant difference at the individual level, which may be a result of the tradition of training and handling domestic horses from the left side [117][87]. The response to vocalisations can also reflect the emotional states and serve a crucial role in the emotional contagion, which could be measured through behavioural observation of the lateralised motor expressions such as ear postures [110,118,119][80][88][89]. Nickel et al. [120][90] reported an asymmetrical movement of the ears in cattle, while Schmied et al. [121][91] observed pendulous ears of cattle during grooming, indicating that they are emotionally aroused and/or positively valenced. Additionally, De Oliveira and Keeling [122][92] predicted that observing the right ear positioned backwards (i.e., asymmetrical right/right ear lateralisation) indicates a positive valence. This prediction is accepting the lateralisation pattern for emotions, as the right side of the body is under the control of the left hemisphere, where the left hemisphere processes positive emotions, such as those of food rewards [117][87]. In addition, the left ear backwards position (i.e., asymmetrical left/left ear lateralisation) indicates negative emotions in cows which has also been studied in different species, such as sheep, horses, cats, and rats, showing the activation of the right hemisphere under stressful situations [123][93]. Also, Siniscalchi et al. [30] reported the involvement of the right ear in the processing of conspecific vocalisations and the left ear in the processing of threatening stimuli. Additional studies have also reported the essential role of the amygdala in the encoding of the olfactory stimuli with affective value [124,125,126][94][95][96]. The lateralisation of the response to stimuli of different valences in the amygdala also indicated that the left amygdala is responsible for positive stimuli and the right for the negative stimuli [127,128][97][98].

4. Relationship between Lateralisation and Behavioural Responses

Limb preference by livestock in locomotion has received increased attention. This limb movement preference was found to be under the control of the motor cortex in the contralateral hemisphere [13], and the lateralised limb preference has been demonstrated in the T-maze and detour test for cattle [129,130][99][100]. The detour task (or directional bias) refers to the direction in which an animal turns around a barrier. This directionality has been used to assess lateralisation preferences in various species [131][101]. The consistency in the direction of movement around the obstacle can be a result of the success of the first choice [132][102]. Lateralisation of movement in horses is continuing to grow as a means of assessing the cognitive and emotional responses. Horses often naturally express a tendency to favour one side or the other when grazing or moving [133][103], indicating individual variations in movement preference. The preferences of horses to choose a side from which they can explore the stimuli has also been studied with regard to potential “optimism”. Individual horses who preferred using the right lateral movement to initiate exploration were more likely to approach new objects in a shorter period of time, suggesting that right-dominant horses are more likely to be more positive (optimistic) [134][104]. Lateralisation assessments have also been employed in cognitive tasks. For example, horses expressed left-side preferences when assessed in cognitive tasks [135][105], and horses with predominantly left-side preference in both sensory and motor behaviours exhibited better problem-solving behaviours and cognitive innovation than those with right-sided preference [113][83]. Motor lateralisation has often been tested through the involvement of obstacles. When horses choose to navigate around an obstacle, they displayed a slight preference for the left-sided navigation, but these lateralisation preferences disappeared as the complexity of the task increased, suggesting that non-lateralised horses may also have better problem-solving capabilities [132][102]. Determining natural motor lateralisation in horses can be complicated due to their history with people. Traditionally, horses are often trained to be led and mounted from the left side, which can impact how they respond to humans and human’s interactions, including husbandry, handling, and riding. There is evidence that the tendency to favour the left lateralisation in movement increases with age [136][106], which could be a function of increased human interaction from the left side. The same is true for how different breeds and ages of horses laterally respond to objects given their history of training [137][107]. Horses naturally have a lateralisation preference which has been shown to be more left-sided preference in domestic horses, more so than in feral horses, which, in addition to being a function of handling, could also indicate increased emotional distress under these conditions [138][108]. Furthermore, even while carrying a passive rider (no active riding aids by the rider), horses showed that the act of carrying a person influences their motor laterality choice, but not the sensory laterality when responding to a novel stimulus [139][109]. Thus, the possibility that some lateralisation could be due to physical growth and genetics, as well as the evidence of biomechanical manifestations of laterality, is limited [140][110]. Therefore, it is important to understand animals’ directional biases which can help in understanding their preferences and their way of interaction with their environment that subsequently highlights their abilities and limitations in the environment [141][111].

5. Relationship between Posture Lateralisation and Behavioural Responses

Lateralisation in the posture of animals has shown to be contradictory in studies. For example, although the lying time in lactating dairy cattle was reported by the authors of [142][112] to be equally divided between the left and right sides, Tucker et al. [62][113] reported that pregnant non-lactating cows showed a preference for the left side, but there was no difference in the lying side preference in cattle in mid and late lactation. Despite these contradictory findings, a shift in the patterns of lying can occur. The preference for lying on the left side had been documented in cattle, in which the authors of [143][114] showed that the percentage of lying time on the left side was higher than the right side in cows and heifers (cows: 64.7 ± 1.1%, and heifers: 61.8 ± 2.7%). However, Bao and Giller [144][115] stated that cows change their sides of lying by about 50–60%. They change their side of lying when the previous lying bout duration increased. Therefore, when there was discomfort from the prolonged lying in one position, they change their side of lying, suggesting that changing sides may alleviate the discomfort. The probability of changing sides in the lying cattle was 50–55% when the previous lying bouts lasted less than 60 min, but this was raised to over 70% when the bouts lasted 80 min or longer. The interval between two successive lying bouts extends to 3 h until the effect of the previous lying bout diminished the ability to determine which side the cow would lie on next. These results indicate that cows avoid lying repeatedly on the same side for longer periods. The differences in lying side preference may be useful for assessing welfare and comfort.

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