The emergence of emotional lateralization: Evidence in non-human vertebrates and implications for farm animals

Applied Animal Behaviour Science 145 (2013) 1–14

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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim

Review

The emergence of emotional lateralization: Evidence in non-human vertebrates and implications for farm animals Lisette M.C. Leliveld a , Jan Langbein a , Birger Puppe a,b,∗ a b

Institute for Behavioural Physiology, Leibniz Institute for Farm Animal Biology (FBN), D-18196 Dummerstorf, Germany Behavioural Sciences, Faculty of Agricultural and Environmental Sciences, University of Rostock, D-18059 Rostock, Germany

a r t i c l e

i n f o

Article history: Accepted 5 February 2013 Available online 5 March 2013 Keywords: Lateralization Hemispheres Emotion Vertebrates Farm animals Welfare

a b s t r a c t The study and protection of animal welfare are based on the assumption that animals are sentient beings, capable of experiencing emotions. Still, our understanding of animal emotions is limited. In this review we focus on the potential of cerebral-lateralization research to provide new insights into animal emotional processing. Thereby, our aims were, first, to find a universal lateralization pattern in emotional processing across vertebrates and, second, to discuss how knowledge of emotional-lateralization patterns can be used in science and practice to contribute to improve farm-animal welfare. A literature review suggests evidence of lateralized functioning during emotional contexts across the vertebrate classes, from early vertebrates such as fish and amphibians to non-human primates. With the possible exception of fish, all vertebrate classes seem to show a similar lateralization pattern for emotional processing, with a right-hemisphere dominance for processing rather negatively connotated emotions, such as fear and aggression, and a left-hemisphere dominance for processing positively connotated emotions, such as those elicited by a food reward. Thus, both hemispheres are involved in emotional processing and hemispheric dominance may be used as an indicator of emotional valence (negative-positive). Although only a few domestic animal species (e.g. chicken, sheep, dog and horse) have been extensively studied with regard to emotional lateralization, evidence gathered so far suggests that the right-hemisphere dominance for fear and aggression and left-hemisphere dominance in responses to food rewards also applies to these species. Such patterns could be exploited in animal welfare studies to gain insight into how an animal experiences a potentially emotional situation and to improve farm-animal management. Further research should focus on rarely-studied species and on rarely-studied emotional contexts, such as sex and positive social situations, to improve our understanding of animal emotional lateralization. © 2013 Elsevier B.V. All rights reserved.

Contents 1. 2. 3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Emotional lateralization in non-human vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Fear/anxiety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author at: Institute for Behavioural Physiology, Leibniz Institute for Farm Animal Biology (FBN), D-18196 Dummerstorf, Germany. Tel.: +49 38208 68812; fax: +49 38208 68802. E-mail address: [email protected] (B. Puppe). 0168-1591/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2013.02.002

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4. 5.

3.2. Aggression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Sex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Responses to food rewards . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Positive social situations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. General pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Implications for farm-animal welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions and outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Understanding animal emotions is of crucial importance for the improvement of animal welfare. Indeed, the assumption that animals are sentient beings, capable of experiencing emotions, such as fear, frustration and pleasure, lies at the base of animal-welfare science and protection (e.g. European Union, 1997; Mendl and Paul, 2004; ˇ Spinka, 2012). Emotions are defined as short-term affective states due to an event (Désiré et al., 2002). Thereby they are distinguished from long-term affective states (moods such as depression), though emotions and moods are inevitably closely connected and influence one another (Mendl et al., 2010). Traditionally the emphasis was on studying ‘discrete’ or ‘basic’ emotions (e.g. fear and aggression; Ekman, 1992). However, recently, researchers have argued that emotional states can be represented as locations in two- or three-dimensional space (core affect; Russell, 2003; Mendl et al., 2010), with valence (positive/negative) and arousal (low/high) as relevant emotional dimensions. The study of emotions is notoriously difficult, especially in non-human animals, since here we miss the most powerful tool: the linguistic self-expression of emotions (Désiré et al., 2002). In animals, assumptions of emotional states are usually derived from behavioural and physiological measurements (e.g. Désiré et al., 2002; Dawkins, 2006). Several researchers have recently argued for a cognitive approach to study emotions in animals (e.g. Mendl and Paul, 2004; Paul et al., 2005). Cognitive approaches facilitate the study of the ‘core affect’ underlying emotions, enabling better categorization of emotions along the valence and arousal dimensions (e.g. Mendl et al., 2010; Zebunke et al., 2011; Puppe et al., 2012). In addition, approaches such as cognitive appraisal (e.g. Désiré et al., 2002, 2004) and cognitive bias (e.g. Harding et al., 2004) provide new insight into the emotional processing of animals. In this paper we promote the idea that the analysis of cerebral lateralization can be useful as part of a cognitive approach to study animal emotional processing. Cerebral lateralization refers to hemispheric asymmetries in structure and/or function (Bisazza et al., 1998). Cerebral lateralization was originally considered to be a uniquely human trait (e.g. Warren, 1980). In recent years, however, extensive evidence has been gathered of structural, functional, and behavioural lateralization in many non-human species ranging from fish to nonhuman primates, indicating ancient evolutionary roots (for reviews see e.g. Bisazza et al., 1998; Rogers, 2002a). Accordingly, all known hemispheric specializations are

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suggested to have evolved from a basic lateralization pattern, common to all vertebrates, in which the left hemisphere is specialized in the control of well-established patterns of behaviour under ordinary and familiar settings and the right hemisphere specialized in detecting and responding to unexpected stimuli in the environment (MacNeilage et al., 2009). In human research, the experience and processing of emotions are recognized to be lateralized processes, but the precise contribution of each hemisphere to emotional processing in humans is still much debated (for reviews see Davidson, 1995; Demaree et al., 2005). Two major hypotheses on lateralized emotional processing are the ‘right-hemisphere hypothesis’ and the ‘emotional-valence hypothesis’ (see Demaree et al., 2005). The ‘right-hemisphere hypothesis’ suggests that the right hemisphere is dominant in all emotional processing (e.g. Gainotti, 1972; Tucker, 1981). The ‘emotional-valence hypothesis’ suggests that the right hemisphere is dominant in the processing of negative emotions, while the left hemisphere is dominant in the processing of positive emotions (e.g. Silbermann and Weingartner, 1986). A variation on this latter hypothesis, by Davidson (1995), postulates that approach-related emotional states are processed with a left-hemisphere dominance, whereas withdrawal-related emotional states are processed with a right-hemisphere dominance (termed the ‘approach–withdrawal hypothesis’). The above mentioned hypotheses are all supported by experimental evidence (e.g. Wylie and Goodale, 1988; Sobotka et al., 1992; Lee et al., 2004). Although lateralized emotional processing has been studied in non-human animals as well (see Rogers, 2002a), it is still not clear whether there is a universal pattern across species that may correspond to one of the emotional-lateralization hypotheses. 2. Approach In this paper our first aim is to provide a comprehensive overview of emotional lateralization across vertebrates, in order to discern a universal pattern and find support for one of the emotional-lateralization hypotheses. The overview serves to show how analysis of cerebral lateralization can provide new insights into emotional processing in animals and, consequently, contribute to the improvement of animal welfare. Earlier reviews showed that cerebral lateralization can provide useful insights into other animalwelfare-related topics, such as animal personalities and coping with stress (reviewed by Morgante and Vallortigara, 2009; Rogers, 2010, 2011). We first review the evidence

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for lateralized emotional processing in non-human vertebrates, focussing more closely on domestic animals. The majority of the reviewed studies use behavioural evidence of lateralized motor expressions or sensory preferences. Such studies rest on the assumption that each hemisphere dominates the control of the contralateral side of the body (Bisazza et al., 1998), so that for example a left eye preference would indicate a greater involvement of the right hemisphere. Based on the literature review, we decided to focus on five major emotional contexts that have been studied with regard to lateralization, namely those associated with fear/anxiety, aggression, sex, responses to food rewards and positive social interactions. The context ‘fear/anxiety’ includes studies that focus on several situations such as the presence of a predator (simulation), facing a potentially life threatening situation (e.g. foot shocks, cold, capture and restraint by humans, or forced swimming), exploration of a novel (fear inducing) space, or the presentation of a novel object (Désiré et al., 2002). The context ‘aggression’ includes studies that observed agonistic conspecific interactions. Thereby we excluded studies that dealt with interspecific predatory attack, which is discussed to be motivationally and neurally different from other forms of aggression (Archer, 1988). The context ‘sex’ includes studies that observed sexual behaviour or presented a sexual stimulus (e.g. othersex conspecifics). The fourth context, ‘responses to food rewards’, includes all studies in which animals respond to the presence of food (predation, food discrimination, food observation). Food is considered to be rewarding to animals and therefore to induce positive emotions (e.g. Boissy et al., 2007). Finally we consider the context general ‘positive social situations’, including studies on play, contact, and observation of conspecifics. A prerequisite here is that the authors provide clear indications that a studied situation is accompanied with positive emotions in the studied subject (e.g. Da Costa et al., 2004). Our second aim in this paper is to consider the implications of lateralized emotional processing in animals on farm-animal welfare. This is discussed in the final part of the review. Thereby we focus not only on the contribution to animal-welfare research, but also on practical implications in animal husbandry.

3. Emotional lateralization in non-human vertebrates Although the existence of conscious experienced emotions is questioned for some, if not all non-human vertebrate species (e.g. Cabanac, 1999; Bermond, 2001), it is interesting to consider the evolution of lateralization in emotional processing, regardless of whether or not this processing is accompanied with conscious emotional experience. For example, studies with early evolved vertebrates on lateralized predator responses (possibly without emotional experience) may provide useful insight into the evolution of the lateralized experience of fear in later evolved vertebrates. Therefore, this review deals with all non-human vertebrate species.

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3.1. Fear/anxiety Most research on emotional lateralization in nonhuman vertebrates has focused on fear/anxiety contexts. Table 1 lists studies providing evidence of lateralization in the fear/anxiety context per vertebrate group, with domestic animal groups shown separately. Several species of bony fish, show lateralized motor responses to predator stimuli (e.g. Bisazza et al., 1997a; Lippolis et al., 2009), which assumingly induce fear. For instance, Lippolis et al. (2009) found that Australian lungfish initiated a flight response by bending head and tail first to the left (C-start), indicating a right-hemisphere dominance. Other species, however showed an opposite bias in their flight response (Heuts, 1999), or had no side bias on a population level, although individual fishes had a strong preference for one side over the other (Bisazza et al., 1997a). Sensory (visual) perception of a predator was also found to be lateralized in many bony fish species. Most species showed a right-eye/left-hemisphere dominance (e.g. Bisazza et al., 2000; Brown et al., 2004), while some species showed an opposite pattern (Bisazza et al., 2000; Budaev and Andrew, 2009). Interestingly, when shoal fish pair-up to inspect a predator, they prefer to use the right eye to view the predator, whereas the left eye is used to view the shoal mate (mirror in the experiment; De Santi et al., 2001, 2002). According to De Santi et al. (2001) observing the shoal mate’s behaviour with the left eye/right hemisphere would allow rapid release of ‘emotional’ flight-or-fight responses. Reddon and Hurd (2009) studied responses of cichlid fish to emotionally conditioned stimuli. The cichlids showed lateralized eye use on an individual, but not population, level for observing an object that was previously associated with an aversive situation (chemical alarm signal). The domestic goldfish showed, like other non-domestic fish species, a left-hemisphere dominance during flight, since goldfishes initiated a flight response with a so-called C-start by bending head and tail to the right (Heuts, 1999). In amphibians, few studies so far focused on lateralized fear/anxiety processing. However, three species of toads showed stronger escape or defensive responses to a predator if it was presented on the left side, suggesting a left-eye/right-hemisphere dominance for fear (Lippolis et al., 2002). In reptiles, evidence of lateralized processing of fear exists for the common wall lizard, of which the majority showed left eye preference during predator inspection (Bonati et al., 2010; Martin et al., 2010). In addition, findings by Deckel (1998) on the Carolina anole suggest an involvement of the right hemisphere in a fear response to human handling. Anoles that were handled prior to an aggressive encounter showed a reduction in left-eye/righthemisphere mediated aggressive movements, compared to unhandled controls, which is explained by the righthemisphere sensitivity to acute stress. In birds, lateralized responses in contexts of fear/anxiety have been studied typically in domestic chickens, of which the findings will be discussed below. The few studies performed so far on other bird species, provide no clear pattern for predator inspection, showing a

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Table 1 Species for which evidence of lateralized processing of fear/anxiety exists. Columns 2 and 3 indicate evidence at population level for left-hemisphere dominance and right-hemisphere dominance, respectively. Column 4 indicates evidence for hemisphere dominance at individual level, not at population level.

Fish

Left hemisphere

Right hemisphere

Individual biases

Brachydanio rerio (29) Brachyrhaphis episcopi (10) Corydoras aeneus (6) Gambusia holbrooki (8, 19) Girardinus falcatus (6, 8, 12, 24) Knipowitschia punctatissima (6) Lepomis gibbosus (6) Padogobius martensi (6) Phoxinus phoxinus (18)

Ancistrus sp. (6) Barbus conchonius (6) Brachydanio rerio (6, 11) Girardinus falcatus (12) Neoceratodus forsteri (38) Pterophyllum scalare (6) Trichogaster trichopterus (6)

Amatitlania nigrofasciata (45) Betta splendens (6) Channa obscura (6) Gyrinocheilus aymonieri (6) Jenynsia lineata (7) Jenynsia multidentata (6) Syngnathus pulchellus (6) Xenotoca eiseni (6)

Amphibians

Reptiles Birds Mammals

Domestic animals Fish Birds Mammals

Junco hyemalis (27) ↓ Macaca mulatta (16) Microcebus murinus (50) Otolemur garnetti (48) Pan troglodytes (36) Rattus norvegicus (13, 55) ↓ Rattus norvegicus (2, 14)

Bufo bufo (37) Bufo marinus (37) Bufo viridis (37) Anolis carolinensis (20) Podarcis muralis (9, 41) Gymnorhina tibicen (30, 34) Callithrix jacchus (31, 32) Callithrix penicillata (56) Macaca mulatta (28, 33) Mus musculus (26) Pan troglodytes (25) Rattus norvegicus (1, 3, 13, 15, 21, 40, 54, 55) Sminthopsis macroura (39)

Carassius auratus (29) Equus caballus (17) ↓ Equus caballus (4)

Gallus gallus domesticus (22, 23, 43, 47, 57) Bos primigenius (46) Canis lupus familiaris (44, 51–53) Equus caballus (4, 5, 17, 35, 49) Felis catus (42)

Equus caballus (4)

↓ indicates evidence of an inhibitory function of the respective hemisphere. References: 1. (Adamec et al., 2003), 2. (Adamec and Morgan, 1994), 3. (Andersen and Teicher, 1999), 4. (Austin and Rogers, 2007), 5. (Austin and Rogers, 2012), 6. (Bisazza et al., 2000), 7. (Bisazza et al., 1997a), 8. (Bisazza et al., 1997b), 9. (Bonati et al., 2010), 10. (Brown et al., 2004), 11. (Budaev and Andrew, 2009), 12. (Cantalupo et al., 1995), 13. (Carlson et al., 1991), 14. (Carlson et al., 1996), 15. (Crowne et al., 1987), 16. (Davidson et al., 1992), 17. (De Boyer Des Roches et al., 2008), 18. (De Santi et al., 2002), 19. (De Santi et al., 2001), 20. (Deckel, 1998), 21. (Denenberg et al., 1978), 22. (Dharmaretnam and Rogers, 2005), 23. (Evans et al., 1993), 24. (Facchin et al., 1999), 25. (Fernández-Carriba et al., 2002), 26. (Filgueiras et al., 2006), 27. (Franklin and Lima, 2001), 28. (Hauser and Akre, 2001), 29. (Heuts, 1999), 30. (Hoffman et al., 2006), 31. (Hook-Costigan and Rogers, 1998a), 32. (Hook-Costigan and Rogers, 1998b), 33. (Kalin et al., 1998), 34. (Koboroff et al., 2008), 35. (Larose et al., 2006), 36. (Leavens et al., 2004), 37. (Lippolis et al., 2002), 38. (Lippolis et al., 2009), 39. (Lippolis et al., 2005), 40. (Maier and Crowne, 1993), 41. (Martin et al., 2010), 42. (Mazzotti and Boere, 2009), 43. (Phillips and Youngren, 1986), 44. (Quaranta et al., 2007), 45. (Reddon and Hurd, 2009), 46. (Robins and Phillips, 2010), 47. (Rogers, 2000), 48. (Rogers et al., 1994), 49. (Sankey et al., 2011), 50. (Scheumann and Zimmermann, 2008), 51. (Siniscalchi et al., 2008), 52. (Siniscalchi et al., 2011), 53. (Siniscalchi et al., 2010), 54. (Sullivan and Gratton, 1999), 55. (Sullivan and Szechtman, 1995), 56. (Tomaz et al., 2003), 57. (Vallortigara et al., 1999).

left-eye/right-hemisphere dominance for Australian magpies (Hoffman et al., 2006), but a right-eye/left-hemisphere dominance for dark eye juncos (Franklin and Lima, 2001). In the latter study, American tree sparrows showed a tendency for a left-eye dominance during predator inspection, but this was not significant. Differences in eye dominance for predator inspection may be explained by emotional appraisal of the predator, as suggested by a study on Australian magpies by Koboroff et al. (2008). In this study, the eye used to observe the predator was correlated to the emotional response of the bird. Inspection with the left eye was usually followed by withdrawal and predator mobbing, whereas inspection with the right eye was usually followed by approach without attacking. Studies with domestic chickens generally suggest a right-hemisphere dominance for the processing of fearinducing stimuli. In young chicks, lesions of the right archistriatum led to a significantly stronger decrease in the production of distress calls (peeps) than identical lesions of the left archistriatum (Phillips and Youngren, 1986).

Furthermore, adult hens were found to scan the air for predators preferentially with the left eye after hearing a conspecific alarm call (Evans et al., 1993), and chicks also preferentially used the left eye to observe aerial predators (Dharmaretnam and Rogers, 2005). Moreover chicks detected a model predator sooner with the left eye (Rogers, 2000) and showed a stronger fear response if they saw the predator with the left eye (Dharmaretnam and Rogers, 2005). The left-eye preference of chicks to observe a novel stimulus (Vallortigara et al., 1999) provides further evidence of a right-hemisphere dominance for the processing of fear. In mammals, a right-hemisphere dominance for the processing of fear and anxiety was demonstrated, for example, by means of unilateral lesions or electrophysiological measurements in rats or mice (e.g. Sullivan and Gratton, 1999; Filgueiras et al., 2006), and measurements of cortical activation, e.g. EEG (Kalin et al., 1998) and tympanic membrane temperature (Tomaz et al., 2003), in non-human primates. Also, behavioural studies showed a

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left-hemimouth/right-hemisphere dominance in the production of facial and vocal fear expressions in primates (e.g. Hook-Costigan and Rogers, 1998a; Fernández-Carriba et al., 2002). For the perception of fear-inducing stimuli marmosets (Hook-Costigan and Rogers, 1998b) and stripefaced dunnarts (marsupial species; Lippolis et al., 2005) showed a right-hemisphere dominance, whereas two prosimian species showed a left-hemisphere dominance (Rogers et al., 1994; Scheumann and Zimmermann, 2008). In addition, some findings suggest that the left hemisphere may be involved in the inhibition of fear (e.g. Davidson et al., 1992; Carlson et al., 1996). In domestic mammals, the evidence for lateralized motor and sensory processing of fear/anxiety has increased in recent years. For example, Quaranta et al. (2007) found that dogs showed asymmetric tail wagging in response to different emotional stimuli. In response to a dominant dog (a fear-inducing stimulus) the dogs showed a more leftward tail wagging. Further evidence of a right-hemisphere dominance in fear processing in dogs was provided by studies on sensory perception. Siniscalchi et al. (2008, 2010, 2011) studied emotional lateralization of dogs in the visual, auditory and olfactory modalities and found that across all three sensory modalities, fear-inducing stimuli (e.g. silhouette image of snake, sound of thunderstorm and the smell of the sweat of the veterinarian) were processed with a right-hemisphere dominance. In addition, in the auditory study (Siniscalchi et al., 2008) they found that left-ear preferences (indicating right-hemisphere dominance) were accompanied with higher reactivity. In cats, the tympanic membrane temperature of only the right ear increased with increasing cortisol serum levels after transport and exposure to a novel environment, indicating a right-hemisphere dominance (Mazzotti and Boere, 2009). Several studies showed right-hemisphere dominance for the visual processing of novel/fear-inducing stimuli in both horses and cattle (e.g. Austin and Rogers, 2007; Robins and Phillips, 2010). Nevertheless, Austin and Rogers (2007) found that when horses were approached by a human with a novel object (umbrella) from the front, the direction of flight was biased on the individual level only, indicating no clear hemisphere dominance for motoric flight response. Moreover, De Boyer Des Roches et al. (2008) found a lefteye bias for observing a veterinarian’s shirt, but a right-eye bias for the novel object (cone), although both are considered to be fear inducing. Interestingly, Austin and Rogers (2007) found that if a horse was presented with the novel object first on its right side, this produced not only lower initial fear responses, but also lower fear responses to subsequent presentations of the object compared to those following an initial left-side presentation, suggesting fear inhibition by the left hemisphere. 3.2. Aggression Evidence supporting lateralized processing of aggression is presented in Table 2. In bony fish, the majority of the studied species showed a population-level righteye-preference during agonistic interactions (Bisazza and De Santi, 2003; Arnott et al., 2011), indicating a lefthemisphere dominance. In contrast, in amphibians a

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right-hemisphere dominance was found in agonistic interactions. Toads and frogs performed tongue strikes at conspecifics, usually guided by the use of the left eye (e.g. Robins et al., 1998; Vallortigara et al., 1998). Also, in reptiles most studies suggest a left-eye/right-hemisphere dominance during aggressive interactions (e.g. Deckel, 1995; Hews et al., 2004). To our knowledge, no evidence of lateralized aggression has yet been reported for birds, with the exception of domestic chickens (e.g. Rogers et al., 1985; McKenzie et al., 1998). In domestic chickens, aggressive behaviour may be accompanied with left-eye use (Rogers et al., 1985; Workman and Andrew, 1986), though findings by Vallortigara et al. (2001) suggest that both eyes are used in different ways during aggressive behaviour combined with social recognition, i.e. the right lateral field and the left frontal field were used during the pecking at strangers, but not at cage mates. McKenzie et al. (1998) found a slightly different result, i.e. the use of the right eye (left hemisphere) allowed inhibition of pecking at a social partner, whereas the use of the left eye did not allow this socially induced inhibition. Several studies found that aggressive behaviour of chicks increased after glutamate treatment of the left hemisphere (e.g. Howard et al., 1980; Deng and Rogers, 1997). Since glutamate causes modification of neural pathways, thereby retarding the normal function of the hemispheres, this suggests that the left hemisphere normally inhibits aggressive behaviour (Howard et al., 1980). In mammals, evidence of lateralized aggression (mainly in primates) indicates a left-hemimouth dominance during the production of facial and focal expressions (e.g. Hauser and Akre, 2001; Wallez and Vauclair, 2011), a lefteye preference during agonistic interactions (Casperd and Dunbar, 1996), and a left-eye/left-ear preference for perceiving aggressive stimuli (Parr and Hopkins, 2000; Basile et al., 2009; but for contradictory findings see: Scheumann and Zimmermann, 2008; Jennings, 2012). Regarding domestic animals, Austin and Rogers (2012) studied feral horses that have not been handled by humans for several generations, and found that these horses show a left-eye preference immediately before or during agonistic interactions. 3.3. Sex Evidence supporting lateralized processing of sex is presented in Table 3. In bony fish, a small majority of the studied species showed a right-eye/left-hemisphere dominance during the observation of other-sex conspecifics (Bisazza et al., 1997b). The right-eye use was also found to increase with increasing sexual motivation (Bisazza et al., 1997b). We found no studies providing evidence of lateralization in the sex context for amphibians and reptiles. In birds, evidence was found for a left-eye/right-hemisphere dominance during sexually motivated behaviour (Japanese quail; Gülbetekin et al., 2007) and during courtship and copulation (blackwinged stilt; Ventolini et al., 2005). However, one further study suggested a right-eye/left-hemisphere dominance during courtship (Zebra finches; Workman and Andrew, 1986).

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Table 2 Species for which evidence of lateralized processing of aggression exists. Columns 2 and 3 indicate evidence at population level for left-hemisphere dominance and right-hemisphere dominance, respectively. Column 4 indicates evidence for hemisphere dominance at individual level, not at population level. Left hemisphere Fish

Birds Mammals

Domestic animals Fish Birds

Anolis carolinensis (10)

Individual biases Betta splendens (6)

Amatitliana nigrofasciata (1) Betta splendens (4) Gambusia holbrooki (4) Xenotoca eiseni (4)

Amphibians

Reptiles

Right hemisphere

Bufo bufo (26) Bufo marinus (20) Litoria caerulea (21) Anolis carolinensis (9, 10) Anolis spp. (8) Sceloporus virgatus (13) Urosaurus ornatus (14)

Dama dama (16) Microcebus murinus (24)

Cercopithecus campbelli (3) Macaca mulatta (12) Pan troglodytes (18, 19) Papio anubis (27) Theropithecus gelada (7)

Gallus gallus domesticus (25) ↓ Gallus gallus domesticus (5, 11, 15, 17, 22, 29)

Gallus gallus domesticus (23, 25, 28)

Equus caballus (2)

Mammals

↓ indicates evidence of an inhibitory function of the respective hemisphere. References: 1. (Arnott et al., 2011), 2. (Austin and Rogers, 2012), 3. (Basile et al., 2009), 4. (Bisazza and De Santi, 2003), 5. (Bullock and Rogers, 1986), 6. (Cantalupo et al., 1996), 7. (Casperd and Dunbar, 1996), 8. (Deckel, 1995), 9. (Deckel, 1998), 10. (Deckel and Jevitts, 1997), 11. (Deng and Rogers, 1997), 12. (Hauser and Akre, 2001), 13. (Hews et al., 2004), 14. (Hews and Worthington, 2001), 15. (Howard et al., 1980), 16. (Jennings, 2012), 17. (McKenzie et al., 1998), 18. (Parr and Hopkins, 2000), 19. (Reynolds Losin et al., 2008), 20. (Robins et al., 1998), 21. (Robins and Rogers, 2006a), 22. (Rogers, 1982), 23. (Rogers et al., 1985), 24. (Scheumann and Zimmermann, 2008), 25. (Vallortigara et al., 2001), 26. (Vallortigara et al., 1998), 27. (Wallez and Vauclair, 2011), 28. (Workman and Andrew, 1986), 29. (Zappia and Rogers, 1983).

In domestic chickens, Rogers et al. (1985) found that sexual behaviour was induced by use of the left eye/right hemisphere, whereas Workman and Andrew (1986) found an opposite effect. The former is supported by findings that glutamate treatment of the left hemisphere increases sexual behaviour in chicks (e.g. Rogers, 1982; Deng and Rogers, 1997), indicating an inhibiting function of the left hemisphere in the sex context.

Some mammalian species also showed lateralized processing in sexually motivated behaviour, however with opposite patterns. The production of copulation screams and grimaces was found to be dominated by the left hemimouth/right hemisphere in rhesus macaques (Hauser and Akre, 2001), while in Mongolian gerbils the production of courtship calls is positively correlated to the size of the sexually dimorphic area in the left hemisphere (Holman

Table 3 Species for which evidence of lateralized processing of sex exists. Columns 2 and 3 indicate evidence at population level for left-hemisphere dominance and right-hemisphere dominance, respectively. Column 4 indicates evidence for hemisphere dominance at individual level, not at population level.

Fish

Amphibians Reptiles Birds Mammals Domestic animals Fish Birds

Mammals

Left hemisphere

Right hemisphere

Individual biases

Gambusia holbrooki (1) Gambusia nicaraguensis (1) Poecilia reticulata (1)

Brachyrhaphis roseni (1) Girardinus falcatus (1)

Betta splendens (3)

Taeniopygia guttata (14)

Coturnix coturnix (5) Himantopus himantopus (13) Macaca mulatta (6)

Meriones unguiculatus (7) Microcebus murinus (9)

Gallus gallus domesticus (14) ↓ Gallus gallus domesticus (2, 4, 8, 10, 15)

Gallus gallus domesticus (11)

Canis lupus familiaris (12)

↓ indicates evidence of an inhibitory function of the respective hemisphere. References: 1. (Bisazza et al., 1997b), 2. (Bullock and Rogers, 1986), 3. (Cantalupo et al., 1996), 4. (Deng and Rogers, 1997), 5. (Gülbetekin et al., 2007), 6. (Hauser and Akre, 2001), 7. (Holman and Hutchison, 1993), 8. (Howard et al., 1980), 9. (Leliveld et al., 2010), 10. (Rogers, 1982), 11. (Rogers et al., 1985), 12. (Siniscalchi et al., 2011), 13. (Ventolini et al., 2005), 14. (Workman and Andrew, 1986), 15. (Zappia and Rogers, 1983).

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and Hutchison, 1993). Also, mouse lemurs showed a rightear/left-hemisphere dominance for the processing of calls of other-sex conspecifics (Leliveld et al., 2010). In contrast, domestic dogs used predominantly the right nostril/right hemisphere (nostrils send their input to the ipsilateral hemisphere) for sniffing the scent of a female dog in oestrous (Siniscalchi et al., 2011).

3.4. Responses to food rewards Evidence supporting lateralized emotional processing in response to food rewards is presented in Table 4. In bony fish, two studied species showed a population preference to strike at prey on their right side (Giljov et al., 2009; Lippolis et al., 2009), indicating a right-eye/left-hemisphere dominance for targeting food. One further study found only individual side preferences for attacking prey (Takeuchi et al., 2012). In their study of cichlid responses to emotionally conditioned stimuli Reddon and Hurd (2009) found that cichlids showed lateralized eye use on an individual, but not population, level for observing an object that was previously associated with an appetitive situation (food). In amphibians, tongue strikes or other predatory responses to prey were mainly guided by the right eye, indicating left-hemisphere dominance for control of feeding behaviour (e.g. Robins and Rogers, 2006b; Giljov et al., 2009). In reptiles, two species, dragon lizards and common wall lizards, were found to show a right-eye/lefthemisphere dominance for feeding as well (Robins et al., 2005; Bonati et al., 2008). Birds also predominantly showed a right-eye/left-hemisphere dominance during feeding (e.g. Alonso, 1998; Ventolini et al., 2005). In domestic birds, the visual discrimination of food from non-food items during feeding was found to be processed with a lefthemisphere dominance in pigeons (Güntürkün and Kesch, 1987) and chicks (e.g. Mench and Andrew, 1986; Deng and Rogers, 1997). In mammals, three out of four studies suggest a righthemisphere dominance for cerebral processing in response to food rewards in primates, as evidenced by a lefthemimouth dominance for the production of food calls (Reynolds Losin et al., 2008) and a left-eye dominance for watching food (Rogers et al., 1994; De Latude et al., 2009; but see: Hook-Costigan and Rogers, 1998b for an exception). Domestic dogs mainly used the left nostril (connected to the left hemisphere) for smelling food (Siniscalchi et al., 2011). In addition, sheep showed a lateralized motor response to food rewards (Reefmann et al., 2009). In response to a better-than-expected food reward and food disappointment sheep had more left-lateralized ears (left ear is more forward than the right ear), indicating right-hemisphere dominance, compared to an expected food reward. Considering the fact that novel stimuli are often experienced as fear inducing (Désiré et al., 2002), the authors suggested that the better-than-expected food reward as a novel stimulus may have been less positive than the expected food reward (Reefmann et al., 2009).

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3.5. Positive social situations Positive social situations have so far been studied rarely with respect to lateralization and we found only evidence for lateralized processing in primates and two domestic mammals (Table 5). The evidence in primates does not provide a clear pattern. Social contact calls were found to be produced with a right-hemimouth dominance in marmosets (Hook-Costigan and Rogers, 1998a), but with a left-hemimouth dominance in chimpanzees (FernándezCarriba et al., 2002) and rhesus macaques (Hauser and Akre, 2001). These latter findings are supported by a left-ear preference for perceiving contact calls in Japanese macaques (Lemasson et al., 2010). Evidence of lateralized processing of positive social stimuli was also provided for domestic dogs and sheep. For instance Quaranta et al. (2007) found that dogs showed a more rightward tail wagging in response to seeing their owner. However, they also showed a rightward bias in response to an unknown human and cats. The authors therefore concluded that their study supported the approach–withdrawal hypothesis, because humans and cats would induce approach, while the dominant dog (as described in Section 3.1) would induce withdrawal. Dogs also showed a right-ear/left-hemisphere dominance for perceiving dog play calls (Siniscalchi et al., 2012). Sheep in isolation showed reduced stress symptoms when presented with sheep faces, compared to goat faces and triangles, suggesting that sheep may find the sight of familiar faces comforting in times of stress, or at least a positive distraction (Da Costa et al., 2004). This presentation was found to reduce mRNA expression of cell-activity-dependent genes in brain regions controlling fear, namely the right central and lateral amygdala, and to increase the expression of these genes in brain regions specialized for emotional control, i.e. the right orbitofrontal and cingulated cortex. Thus, this study shows that fear-related neural activity in the right hemisphere can be reduced by a positive social stimulus (familiar face). Finally, Versace et al. (2007) found that both adult sheep and lambs go around a centrally placed obstacle on the right side to re-join flock mates (adults) or their mother (lambs). According to the authors, this bias is caused by a preferential turning of the head to the right to fixate the target, i.e. flock mates or mother, in the left hemifield, suggesting a left-hemifield/righthemisphere dominance for viewing familiar individuals. The authors suggested that at least the lambs had a strong motivation to return to their mother, which implies a right-hemisphere dominance for processing positive social stimuli. In addition, a right-hemisphere dominance was found in the processing of social stimuli in general, without referring to its emotional valence, for instance during social recognition (e.g. Daisley et al., 2009; Deng and Rogers, 2002) and imprinting (Johnston and Rogers, 1998). 3.6. General pattern Overall it can be concluded that emotional lateralization is universal across vertebrates. Although a clear overview was not always found for each class, some general patterns could be discerned. For instance, fear/anxiety and

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Table 4 Species for which evidence of lateralized processing in response to a food reward exists. Columns 2 and 3 indicate evidence at population level for lefthemisphere dominance and right-hemisphere dominance, respectively. Column 4 indicates evidence for hemisphere dominance at individual level, not at population level. Left hemisphere Fish Amphibians

Reptiles Birds

Mammals

Domestic animals Fish Birds Mammals

Perccottus glenii (6) Neoceratodus forsteri (10) Bufo bufo (23) Bufo marinus (16, 23) Bufo viridis (23) Pleurodeles waltl (6) Ctenophorus ornatus (15) Podarcis muralis (2) Coturnix coturnix (22) Dacelo gigas (17) Himantopus himantopus (24) Taeniopygia guttata (1) Callithrix jacchus (8)

Columba livia f. domestica (7) Gallus gallus domesticus (4, 5, 9, 11, 18, 25) Canis lupus familiaris (20) Ovis aries (13)

Right hemisphere

Individual biases Amatitlania nigrofasciata (12) Perissodus microlepis (21)

Bufo marinus (16)

Dacelo gigas (17)

Cercocebus torquatus (3) Otolemur garnetti (19) Pan troglodytes (14)

Ovis aries (13)

References: 1. (Alonso, 1998), 2. (Bonati et al., 2008), 3. (De Latude et al., 2009), 4. (Deng and Rogers, 1997), 5. (Dharmaretnam and Rogers, 2005), 6. (Giljov et al., 2009), 7. (Güntürkün and Kesch, 1987), 8. (Hook-Costigan and Rogers, 1998b), 9. (Howard et al., 1980), 10. (Lippolis et al., 2009), 11. (Mench and Andrew, 1986), 12. (Reddon and Hurd, 2009), 13. (Reefmann et al., 2009), 14. (Reynolds Losin et al., 2008), 15. (Robins et al., 2005), 16. (Robins and Rogers, 2006b), 17. (Rogers, 2002b), 18. (Rogers and Anson, 1979), 19. (Rogers et al., 1994), 20. (Siniscalchi et al., 2011), 21. (Takeuchi et al., 2012), 22. (Valenti et al., 2003), 23. (Vallortigara et al., 1998), 24. (Ventolini et al., 2005), 25. (Zappia and Rogers, 1987).

aggression seem to be predominantly processed by the right hemisphere in most classes, with the clear exception of fish (see Tables 1 and 2). Cabanac (1999) suggested that emotions evolved somewhere between amphibians and reptiles, since he found that rats and lizards, but not frogs and fish, showed signs of emotional fever and tachycardia in response to handling. Thus, the right hemisphere may only become dominant in the processing of responses when situations such as predator observation and agonistic interaction are accompanied by the experience of intense emotions. Indeed, it has been suggested that the left-hemisphere dominance of some fish species in these situations reflects that the fish are carefully assessing the situation, rather than responding emotionally (De Santi

et al., 2001; Bisazza and De Santi, 2003). Alternatively, the methods used in the fish studies may partially explain the left-hemisphere dominance at least for the fear/anxiety context. In this context most studies on fish have used the detour task (the subject has to detour a barrier either to the left or right in order to view a stimulus; Bisazza et al., 1997b), which involves the subject approaching and inspecting a predator (De Santi et al., 2001). Such an action is more likely to involve careful planning and inhibition of an emotional response, compared to startle responses, as studied in other vertebrate species. Indeed, there is evidence to suggest that the left hemisphere may play an important role in the inhibition of fear and anxiety (e.g. Davidson et al., 1992; Adamec and Morgan, 1994; see also:

Table 5 Species for which evidence of lateralized processing of positive social situations exists. Columns 2 and 3 indicate evidence at population level for lefthemisphere dominance and right-hemisphere dominance, respectively. Column 4 indicates evidence for hemisphere dominance at individual level, not at population level. Left hemisphere

Right hemisphere

Fish Amphibians Reptiles Birds Mammals

Callithrix jacchus (4)

Macaca fuscata (5) Macaca mulatta (3) Pan troglodytes (2)

Domestic animals Fish Birds Mammals

Canis lupus familiaris (6, 7)

Ovis aries (1, 8)

Individual biases

References: 1. (Da Costa et al., 2004), 2. (Fernández-Carriba et al., 2002), 3. (Hauser and Akre, 2001), 4. (Hook-Costigan and Rogers, 1998a), 5. (Lemasson et al., 2010), 6. (Quaranta et al., 2007), 7. (Siniscalchi et al., 2012), 8. (Versace et al., 2007).

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Andrew and Rogers, 2002), though this evidence is so far restricted to mammals. Responses to food rewards seem to be predominantly processed by the left hemisphere, except in primates (see Table 4). Two of the reviewed studies with primates involved observations of food, not the actual act of feeding (Rogers et al., 1994; De Latude et al., 2009), and the exception could be due to a different emotional experience, for example involving frustration caused by seeing food without being allowed to eat it. The left-hemisphere’s dominance in responses to food rewards may be closely linked to its specialization for categorization, as is most apparent in food-discrimination studies (e.g. Deng and Rogers, 1997; Alonso, 1998), or to its role in predation (e.g. Robins et al., 2005; Giljov et al., 2009). For sex and positive social situations, no clear pattern could be found (see Tables 3 and 5), which is probably due mainly to the fact that these types of emotional lateralization have been little studied. Positive social situations will proof challenging to study in many species, since often it is difficult to ascertain the positive nature of a social situation. Complicating the study of the ‘sex’ context is that sex (including courtship) relates to different emotions, which generally are considered to be positive (Hauser and Akre, 2001; Boissy et al., 2007), but may include those associated with aggressive competition (Hauser and Akre, 2001). The emotional valence in the sex context may therefore depend on the presence or absence of competition, which varies between situations, individuals and species. Moreover, similarly to the ‘fear/anxiety’ context, the conflicting results in the ‘sex’ context may also result from different paradigms as some studies focused on courtship or observation of other-sex conspecifics, while others focused on copulation. The general pattern of right-hemisphere dominance in processing fear/anxiety and aggression, and lefthemisphere dominance in processing responses to food rewards, does not support the ‘right-hemisphere hypothesis’ (e.g. Gainotti, 1972; Tucker, 1981), which assumes that all emotions are processed by the right hemisphere. Also, there is no strong support for the ‘approachwithdrawal hypothesis’ (Davidson, 1995), since fear (associated with withdrawal behaviour) and aggression (associated with approach behaviour) are both processed with the right hemisphere. The ‘emotional-valence hypothesis’ (e.g. Silbermann and Weingartner, 1986) may best explain the findings reviewed here, since responses to food rewards (of positive emotional valence) are associated with a left-hemisphere dominance, while fear and aggression (of predominantly negative emotional valence) are associated with a right-hemisphere dominance. Still, the left-hemisphere dominance in regulating responses to food rewards could be ascribed not only to the positive emotional valence elicited by food, but also to other (non-emotional) cognitive processes, such as categorization, meaning that no definite conclusion can be drawn until more evidence of lateralized processing during positive social situations is provided. For now, we can conclude that the right hemisphere is dominant in the processing of predominantly negative emotions, while the left hemisphere is dominant in responses to food rewards. Thereby this observed pattern of emotional lateralization is in line

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with general lateralization patterns (e.g. Rogers, 2002a; MacNeilage et al., 2009), in which the left hemisphere specializes in considered/reflective responses to familiar stimuli, whereas the right hemisphere specializes in rapid/reflexive responses to novel and unexpected stimuli. The lateralization patterns found for domestic species seem to be in accordance with the lateralization patterns of non-domestic species. The right-hemisphere dominance for fear and aggression and the left-hemisphere dominance in responses to food rewards are supported here by findings in chickens, horses, dogs, cats, pigeons, cattle and sheep. Nevertheless, convincing evidence is still missing from many domestic animal species for most of the emotional categories and the understanding of lateralization in emotional processing in all domestic species necessitates further studies. 4. Implications for farm-animal welfare The knowledge of cerebral lateralization in farm animals is rapidly increasing. There are indications of various forms of cerebral lateralization, other than emotional, in chickens (e.g. Andrew et al., 2004), horses (e.g. McGreevy and Rogers, 2005), cattle (e.g. Tucker et al., 2009), donkeys (Zucca et al., 2011), goats (Langbein, 2012) and sheep (e.g. Morgante et al., 2007). Such knowledge allows a better understanding of the cognitive functioning of these animals and may provide novel approaches to improve their welfare (reviewed by Morgante and Vallortigara, 2009; Rogers, 2010, 2011). Specifically, behavioural manifestations of lateralization could give insight in the valence of an emotion that an animal experiences, which would facilitate the categorization of the emotion along valence and arousal dimensions and thereby the study of its ‘core affect’ (Mendl et al., 2010; Puppe et al., 2012). Moreover, like other cognitive approaches (e.g. Désiré et al., 2004; Harding et al., 2004), indicators of lateralization can provide insight into the cognitive processing of emotions. In this section we discuss the implications of emotional lateralization on farm-animal welfare (research). The review above indicates a right-hemisphere dominance for the processing of predominantly negative emotions, such as fear, novelty and aggression. This pattern could be exploited in studies on animal welfare, by means of using indicators of right-hemisphere dominance for identifying negative emotional states. For example, in their study on sheep, Reefmann et al. (2009) initially predicted that an unexpected, enriched food reward would cause more positive emotions compared to an expected, normal food reward. However, lateralization in the ear postures suggested a slightly stronger right-hemisphere involvement for the enriched food compared to the expected food reward. This pattern, combined with other behavioural indicators of negative emotional states, led the authors to conclude that the enriched food (as a novel stimulus) is experienced as less positive than the expected (but not enriched) food. The lateralization pattern also mirrors how individual animals cope with a certain emotional event, like the increased fear-related right-hemisphere dominance with increased emotional reactivity of the subject (e.g. Larose et al., 2006; Siniscalchi et al., 2008). Dominance

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by the left hemisphere may indicate that the animal is not emotional and possibly in control of the situation, as demonstrated in wild Australian magpies (Koboroff et al., 2008), which used the right eye before approaching a model predator for closer inspection (without attacking it). Thus, the lateralization pattern may help to determine whether an animal experiences certain situations as emotionally negative (e.g. Morgante and Vallortigara, 2009; Rogers, 2010), depending on the animal’s personality or treatment, and on whether the situation is controllable. Additionally, cerebral lateralization may be an important factor to take into account when studying emotional contagion (the transfer of an emotional state from one animal to another; ˇ Spinka, 2012), as animals may be affected by this to a different degree depending on the dominant hemisphere with which the emotion is perceived. It remains to be tested if perception with the right hemisphere makes the animal more susceptible to contagion of negative emotions, and perception with the left hemisphere for contagion of positive emotions. In studies on animal emotions cerebral lateralization can be measured relatively easily and non-invasively. As shown above, cerebral lateralization could be measured by behavioural observations of lateralized motor expressions of emotions, such as ear postures in sheep (Reefmann et al., 2009) or tail wagging in dogs (Quaranta et al., 2007). Such measurements are species dependent as different species express their emotions in different ways. Other types of motor lateralization, such as limb preferences may also be influenced by the affective state of the animal (e.g. Zucca et al., 2011) and therefore be indicative of it. However, in behaviours that are not direct expressions of emotions, other factors may also influence the lateralization pattern, making them less reliable measurements of lateralization. Visual lateralization may also be easily observed during emotional situations, at least in animals with laterally placed eyes, e.g. horses (Austin and Rogers, 2007), cattle (Robins and Phillips, 2010) and chickens (Rogers, 2000). In such cases the eye turned towards the tested emotional stimulus may be taken as a measure of cerebral lateralization. Nostril preference may also be directly observed, providing that the animal’s nostrils are easily distinguishable during sniffing, e.g. horses (De Boyer Des Roches et al., 2008). Alternatively, lateralization patterns may be determined by blocking subsequently the left or right eye, ear or nostril, and comparing the difference in response (e.g. Deng and Rogers, 2002). In addition, special tests may be used to measure lateralization, such as a detour test for visual processing (e.g. Vallortigara et al., 1999) or a head-turn test (e.g. Siniscalchi et al., 2008) for auditory processing. Finally, non-behavioural measurements, such as electroencephalography (EEG; e.g. Davidson et al., 1992), tympanic membrane temperature (e.g. Mazzotti and Boere, 2009) or functional near-infrared spectroscopy (Gygax et al., 2013) may also be used to detect cerebral lateralization in emotional situations. Knowledge of emotional-lateralization patterns could also be exploited in farm management, such as during the handling of animals. Levels of fear and aggression could be reduced if the animal is handled from the correct side, which would improve human–animal interactions and,

consequently, animal welfare. The exact practical application of this knowledge is, however, not always clear, as is illustrated for horses. On the one hand, the preferential use of the right hemisphere to process fearful situations has led Larose et al. (2006) to suggest that horses may prefer to be approached and mounted from the left side. This suggestion was supported by Farmer et al. (2010), who found that horses preferred to view humans with their left eye. On the other hand, the finding of a left-hemisphere inhibition of fear responses has led Austin and Rogers (2007; see also Rogers, 2011) to conclude that horses would be more relaxed and learn faster if they are handled and approached from the right side. These contradicting views show that there is a great need for studies on emotional lateralization in everyday situations, such as during human–animal interactions. Lateralized responses to food rewards may also have practical advantages in farm management. Animals may feed more readily if food is presented from their right side, allowing a greater involvement of the left hemisphere during feeding. However, a study on dairy cows by Rizhova and Kokorina (2005) suggests that the wellbeing and also performance of animals may be improved if the food is presented to them from the left side. In this study they discovered that the direction from which food was delivered to the cows, on a food belt, affected their reproductive success and milk production. Cows that received food from the left side (so that the food was processed first by the right hemisphere) every day for several months had increased reproduction success, compared to cows that received food from the right side every day. Lateralized effects on milk production depended on the feeding conditions of the herd, with left side food presentation increasing milk production under good feeding conditions and right side presentation increasing milk production under poor feeding conditions. This study suggests the existence of a link between the processing of positive stimuli (food), and somatic processes that control reproduction in the cow right hemisphere. Thus, cerebral lateralization research may provide practical applications to improve farm-animal welfare as well as financial gain for the farmers. 5. Conclusions and outlook The present paper shows that there is ample evidence of lateralization in emotional processing across vertebrate species. Fish seem to be the odd ones out, as they tend to show more involvement of the left hemisphere in situations linked to fear and aggression. This may reflect an absence (or inhibition) of emotional appraisal during intrinsically emotional situations (e.g. presence of predator), but may also be explained by methodology. Across the other vertebrate classes a general pattern is discerned of a right-hemisphere dominance for rather negatively connotated emotions (fear and aggression), and a lefthemisphere dominance for positively connotated emotions (at least with regard to responses to food rewards). Thus, both hemispheres partake in the regulation of an animal’s emotional state and the relative dominance between the hemispheres reflects the valence of the emotion. This finding provides support for the ‘emotional-valence

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hypothesis’ rather than for alternative hypotheses. Lateralization may therefore provide important insights into emotional processing in animals, facilitating the categorization of emotions along the valence dimension. The aforementioned general pattern of emotional lateralization is also evident in domestic animals, mainly chickens, horses and dogs. Nevertheless, evidence is still missing from many farm animal species for most of the emotional categories. In order to improve our understanding of emotional lateralization in farm animals, studies also need to focus on yet unstudied species, such as pigs. Moreover, our knowledge of emotional lateralization in farm animals is often limited to the fear context and studies are needed that focus on other emotional contexts, such as aggression, sex, responses to food rewards and positive social situations, in order to better understand emotional lateralization within a species. Knowledge of emotional lateralization in farm animals could increase the understanding of their emotions as well as of how they cognitively deal with them. Specifically, knowledge of cerebral lateralization may help to increase our understanding of the link between emotions and cognitive processing, facilitating cognitive approaches to study emotions. It could also be directly exploited in farm management to improve animal welfare, such as during human–animal interactions. Knowledge of an animal’s emotional-lateralization pattern can help to reduce negative emotional experience during farm management procedures by, for example, handling the animal from the correct side. However, the few publications that have focused on such practical implications show that the best application of emotional lateralization knowledge is not always clear, which underlines the value of future studies on the role of emotional lateralization in farmmanagement practises. Acknowledgements The study was supported by the grant 0315536G from the German agriculture network PHÄNOMICS (funded by the Federal Ministry of Education and Research). Thanks to Sandra Düpjan, Heinz Deike, Katrin Siebert, Dagmar Mähling and Evelin Normann for their technical support in preparing preliminary experiments in pigs. We also thank Sharon Kessler for polishing the English and the anonymous referees for their helpful comments and advice. References Adamec, R.E., Blundell, J., Burton, P., 2003. Phosphorylated cyclic AMP response element binding protein expression induced in the periaqueductal gray by predator stress: its relationship to the stress experience, behavior and limbic neural plasticity. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 27, 1243–1267. Adamec, R.E., Morgan, H.D., 1994. The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physiol. Behav. 55, 1–12. Alonso, Y., 1998. Lateralization of visual guided behaviour during feeding in zebra finches (Taeniopygia guttata). Behav. Proc. 43, 257–263. Andersen, S.L., Teicher, M.H., 1999. Serotonin laterality in amygdala predicts performance in the elevated plus maze in rats. Neuroreport 10, 3497–3500.

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