1

Pain and emotions in non-human animals:

Debates and insights from philosophy, ethology and neuroscience

Dolore ed emozioni negli animali:

Dibattiti e prospettive in ambito filosofico, etologico e neuroscientifico

Abstract

The experience of pain can be referred verbally by human subjects and, although this criterion is considered during scientific and medical procedures, it appears evident that the same principle cannot be applied to other species. Thus, pain in animals is usually inferred by non-verbal behaviors, but this inference is not, or should not be that simple to make. In the present work available philosophical, ethological and neuroscientific resources about the experience of pain in humans and animals will be reviewed, to explore continuities and specificities by a comparative perspective. Also, a new framework will be proposed to highlight some significant behaviors related to pain experience within the animal kingdom. In detail, we suggest that by observing and analyzing complex emotional and social (shared) experiences related to pain it would be possible to infer, at least in some cases, the presence of a subjective experience of pain.

Keywords

Pain; Emotions; Animals; Human being; Empathy

Riassunto

I criteri standard per valutare la presenza di esperienze legate al dolore prevedono un riscontro verbale da parte dei soggetti (umani) coinvolti. Tuttavia, mentre questo tipo di informazioni vengono normalmente considerate durante procedure mediche e scientifiche, appare evidente che lo stesso tipo di indagine non può essere effettuata nel caso degli animali non umani. A questo proposito sono stati sviluppati alcuni metodi per

2

dedurre la presenza di dolore tramite la valutazione di indizi non verbali, anche se simili inferenze non sono, o quantomeno non dovrebbero essere, così facili da fare. Lo scopo del presente studio è quello di raccogliere le principali evidenze filosofiche, etologiche e neuroscientifiche sull'esperienza del dolore nell'uomo e negli animali, per esplorare la presenza di continuità e specificità da una prospettiva comparativa. Inoltre, verrà proposta una nuova cornice interpretativa che possa aiutare a cogliere alcuni comportamenti significativi legati all'esperienza del dolore nel regno animale. Più specificamente, proponiamo l’osservazione e l’analisi di esperienze emotive e sociali complesse (e condivise) come strumento per dedurre, almeno in alcuni casi, la presenza di un'esperienza soggettiva di dolore.

Parole chiave

Dolore; Emozioni; Animali; Esseri umani; Empatia

3

Introduction: The problem of consciousness

Do animals (and to what extent) feel pain? The complexity of such question has led to a relative paucity of research and controversial evidence on the subject. In fact, the differences occurring between ours and other species and the linguistic obstacle make the discussion difficult at many different levels. Thus, research on this topic often had to face concerns about anthropomorphism, the tendency to attribute human motivations and feelings to other animals. On the other hand, these concerns diverted towards the opposite position, that has been called by de Waal as anthropodenial (1997), the blindness to the humanlike features of other animals, and vice versa (see also Mogil, 2015).

One solution that was adopted when trying to recognize pain experience to animals involved defending a particular theory of animals’ consciousness. However, this new topic does not seem to clarify the question much. In fact, conventional behavioral indices to attest human consciousness relies on the abilities to refer events with accuracy (Seth, Baars, & Edelman, 2005). However, while this method is usually applied for scientific and medical applications in humans, it appears evident that the same criteria based on verbal language could not be generalized to other species.

Recently, an important step was moved towards the awareness that humans are not unique in possessing the neurological substrates that generate consciousness, and that it is also widespread within the animal kingdom. This step consists in the Cambridge Declaration on Consciousness. The Declaration was publicly proclaimed at Cambridge, on July 7, 2012, at the Francis Crick Memorial Conference on Consciousness in Human and non-Human Animals, held at Churchill College, University of Cambridge. Here, a group of brain scientists declared that “Convergent evidence indicates that non-human animals have the neuroanatomical, neurochemical, and neurophysiological substrates of conscious states along with the capacity to exhibit intentional behaviors” (Low, 2013).

Starting from this point, important issues can be considered about animals’ pain. In fact, as already happened in the case of humans, the disposition about pain in animals is evolving. For example, an interesting anecdote has been reported by Pernick (1985) who documented that in Pennsylvania during the 1860s about 30% of amputations on human patients were conducted without anesthesia, despite the availability of drugs at low cost. Anesthesia, indeed, was reserved only for those patients

4

who were considered most sensitive to pain: whites, women and rich people. On the other hand, immigrants, black and poor people, as well as the uneducated and alcoholics were thought to be insensitive (Weary, Niel, Flower, & Fraser, 2006). Of course, thanks to scientific and cultural progress, nowadays we know much more about the pain experience in humans, regarding both objective and subjective issue.

However, it is important to clarify what we mean with animals’ consciousness, possibly an even tougher problem. A traditional distinction refers to phenomenal and access consciousness. The first one can be described as pure experience and is more frequently thought to be shared also by non-human animals, while the second one involves availability for rational control and, thus, it is more rarely attributed to animal kingdom. However, as already pointed out by Tye (2016) and Godfrey-Smith (2016), this distinction is not useful and could be simplified by suggesting that “a being is conscious just in case it undergoes experiences” (Tye, 2016). As the author himself admits this view, although simple, is usually rejected. In Godfrey-Smith’s opinion, consciousness could be considered in its broader meaning to define all those forms of integrated and organized subjective experience. From a phylogenetical point of view, it is probable that this kind of experience emerged along many different evolutionary pathways through simple and ancient forms (Godfrey-Smith, 2016). Thus, the problem of animal consciousness becomes more easily addressable by considering animal experiences in general. In fact, we share Godfrey-Smith’s idea (2016) that it seems unlikely that pain suddenly appear in its final form in humans. For example, Cabanac and colleagues (Cabanac, Cabanac, & Parent, 2009) proposed that the first mental event to get into consciousness was the capacity to distinguish between pleasure and displeasure, thus creating a strong link to emotional experience. However, they hypothesize the emergence of an emotional life between amphibians and early reptiles, thus excluding fish and insects.

An in-depth discussion of the concept of consciousness and its declensions in the animal kingdom is not part of the purposes of the present study. However, even if it represents a bold step with regard to previous perspectives, we believe that this last definition can allow a broader and more empirical treatment of the problem, thus providing at least some initial clues to go deeper into the main issues.

Definitions and caveats

5

Focusing specifically on pain experience, it is important to provide a definition to properly address the problem. Another distinction has been drawn here between nociception and pain experience, which describes the first one as a non-conscious neural processing of stimuli that could cause body tissue damage (noxious stimuli). This process is accompanied by specific motor behaviors, called nociceptive behaviors, which in general are reflex responses and are executed non-consciously (Key, 2016) to terminate such perception. In this light, nociception can be considered as one of the most primitive sensory capacities, in that neurons functionally responsible for nociception have been described also in invertebrates (Allen, 2004). Thus, nociception appears to be shared by humans and non-human animals. However, although in humans reflex withdrawal responses following a nociceptive stimulus generally correlate with subjective experience of pain, as reported verbally, the distinction between nociception and pain experience is not always clear in non-human animals (National Research Council, US, Committee on recognition and alleviation of pain in laboratory animals, 2009).

According to Key’s position (Key, 2016), the feeling of pain in humans emerge at long latencies, since it involves supraspinal neural pathways leading to evoked brain potentials (Bromm & Lorenz, 1998; Garcia-Larrea, Charles, Sindou, & Mauguiere, 1993) that are associated with conscious neural processing (Boly et al., 2011; Changeux, 2012; Constant & Sabourdin, 2015). Nonetheless, recent perspectives consider this distinction as misleading, and a relic of attempts to stress differences between humans and other animals, or between "higher" and "lower" animals (Broom, 2016). In fact, according to Broom, the use of the term nociception, which separates one part of the pain system from other parts, should be suppressed since it is questionable and creates a hierarchical model of pain. Moreover, Wall suggested that the debate around pain in humans and non-human animals is often “confused by the pseudoscience surrounding the word nociception” (Wall, 1979)(PAG). Accordingly, the pain system should be considered as a whole (Broom, 2014; Wall, 1992).

Therefore, what about pain experience? Is it a prerogative of just human beings? The complexity of this second point requires a deep analysis. About human beings, pain can be described as “an unpleasant sensory and emotional experience associated with actual or potential tissue damage or described in terms of such damage” (IASP, 1979; p. 250). Of course, given the presence of a subjective, private dimension, a question arises about our capacity to really understand the emotions experienced by another being,

6

especially in the case of animals that cannot provide narrative evidence (Weary et al., 2006). Considering the same topic with regard to animals, one definition that was proposed concerned “an aversive sensory experience caused by actual or potential injury that elicits protective motor and vegetative reactions, results in learned avoidance and may modify species-specific behaviors, including social behavior” (Zimmerman, 1986; p. 1). This definition was later modified by Broom (2001) who preferred the use of the word “feeling” (p. 17). This term eliminates the implication of the concept of awareness. Accordingly, a feeling is defined as a brain construct involving at least perceptual awareness. It is associated with a life regulating system, it can be recognized by the individual and may change behavior with learning processes to minimize painful experiences in the future. This view highlights two significant points. First, pain is a private experience. Second, pain can be considered an adaptive mechanism in both humans and non-human animals. In fact, it can be thought as a tool to help us cope with aversive events during life.

In fact, there is evidence that some animal species, among which also all vertebrates and some invertebrates, need a certain level of pain and other feelings to effectively respond to their environment and thus survive. Indeed, nociception can be considered as an evolutive mechanism, a withdrawal behavior from potentially threatening stimuli that can cause damage to the organism (Elwood, 2018). Similarly, it is possible to hypothesize that pain, as well, could have had some further benefits, such as the creation of emotional memories and long-lasting motivations towards the adoption of more adapted functioning (Bateson, 1991). In this perspective, we could hypothesize the presence of pain experience in non-human animals, since painful stimuli and emotions are able to modify animals’ intentions and behavioral patterns. Also, since pain and fear systems are phylogenetically old, it could be considered implausible that they have suddenly emerged in mammals or in humans (Broom, 2016).

However, a cautious definition that seems completely suitable in the case of animal pain, is that it merely corresponds to that “sentience, sensation, and feeling that humans can understand through observing either behavior or the lack of behavior”, thus stressing the presence of an interpretative leap (Mroczek, 1992; p. 28).

According to the definitions reported above, feelings of pain in nonhuman animals can be assessed by physiological responses and direct behavioral observations, including the ability to learn from aversive

7

experiences in order to display modified, adapted behaviors in the future (Broom, 2001).

Another construct that is often considered when dealing with pain experience is that of suffering. It is an even more complex concept that goes beyond physical pain, and can be defined as an “enduring negative emotional state associated with a perceived sustained threat to the integrity of the individual, helplessness, or isolation from significant others” (Chapman, 1992). Although sometimes the term was used synonymously with pain, suffering can also manifest merely psychologically and can, thus be present without physical pain. At the same time, it is possible to experience pain without suffering. Just think about the sadomasochistic procedures (Rowan, 1988). Some interesting evidence has been collected with regard to suffering in non-human animals, especially by observing the effects of the alleviation of boredom. Just think about the animals in cages and the effects of captivity on their natural behavior (Elwood, 2018). However, the theme of suffering in animals goes beyond the scope of the present work, which will especially focus on pain experience (however, for an interesting overview on the relationship between pain and suffering in animals see Aitken, 2008).

In the following sections some significant philosophical perspectives in favor or against the capacity of animals to feel pain will be discussed; also, highlights on pain systems from a physiological point of view will be provided. Additionally, some important concerns on phylogenetic specificities will be considered, together with some evidence of complex pain experiences in different species of interest. Finally, moral and ethical matters will be presented at light of what previously discussed.

Do non-human animals feel pain? Answers from philosophy

As can be noted also from previous paragraphs, the positions on animal pain tend to be in general at one extreme or another, thus leading to reductive views. In fact, considering the philosophical perspective, from one side there are those who think that the similarities between humans and other non-human animals lead directly to the fact that these second can

8

experience pain consciously in exactly the same way as we do. On the opposite side there are those who think that animals can’t experience pain consciously at all, or that they can experience “lower” or different forms with respect to human beings (Allen, 2004).

For what concerns the first approach, according to Allen’s paper (2004), philosophical evidence provides two basic arguments to defend the view that non-human animals can experience pain, emotions, or other sensations consciously, and in the same way as humans. The first one is inferential and affirms that the presence of mental states is based on the perceived similarity between humans and other animals, with respect to behavioral, anatomical, and physiological features. This approach is typically supported by claims about evolutionary continuity. On the other hand, the second approach is non-inferential and maintains that our knowledge of animal consciousness derives from our direct interactions with them (Searle, 1994). According to this point of view, Searle argued: “I do not infer that my dog is conscious, any more than, when I came into this room, I inferred that the people present are conscious. I simply respond to them as is appropriate to conscious beings. I just treat them as conscious beings and that is that” (Searle, 1994).

The inferential approach is usually discussed by analogy, such that conscious experience in humans is related to a specific property, and then it is concluded that other animals possessing the same property could be considered conscious in the same way. Arguments set in this form are those mostly used, for example, in the field of animal rights and animal welfare. As already discussed above, a similar perspective was also proposed by Tye (2016), which affirmed that, when witnessing what we consider a pain experience in animals, “a simpler hypothesis has to be preferred, unless there is evidence that challenges the inference” (p. 74).

However, the analogy argument is often weak to sustain: in fact if it’s true that a number of similarities bond humans and non-human animals, it is equally true that a number of dissimilarities can be used to deny these inferences in the same way (Nelkin, 1986). This can be applied to both overt behavior and neurological features: in the first case, our behavior cannot be identical to that of other animal species, so it is possible to emphasize the differences, insisting, for example, on linguistic criteria for consciousness. In the second case, the question is whether the neurophysiological differences between nonhuman animals and humans provide a solid defeater to the analogy, given the behavioral similarities (see further on).

9

Within the philosophical frame, still according to Allen (2004), two formalized theories about conscious experience of pain deserve special attention: the promoters of such theories are Tye (2000) and Carruthers (2000). Tye described the pain experience as the result of immediate sensory representations that can influence beliefs or desires. To provide evidence that animals experience conscious pain, like Broom (2016), Tye focused on changes in believes or desires manifested through non-reflexive behaviors in response to nociceptive stimuli, and cited some examples in a variety of different animal species that show flexible and goal-driven behaviors. Nevertheless, despite supporting a first-order account of consciousness in animals, Tye also maintained that “simple creatures” never suffer, in that suffering requires the cognitive awareness of pain (Tye, 2000, p. 182). Thus, he raised a higher-order account of suffering which seem to be inaccessible to most of non-human animals.

In the same period, Carruthers (2000) developed a higher-order theory of consciousness as well, which was used, in this case, as a basis argument against any form of conscious pain experience in animals. In fact, according to Carruthers’ theory, phenomenal consciousness requires the capacity to think about, and consequently conceptualize, one’s own thoughts. More precisely, it is required that the subject has a theory of mind (ToM) and, according to Carruthers’ point of view, non-human animals don’t possess this capacity. Nonetheless, also in this case, it is important not to deal with the attempts to attribute similarities with human-like behaviors within an anthropocentric point of view, but to consider all possible factors that could intervene in those protocols that have been conceived for humans.

This kind of studies on self-consciousness and ToM in non-human animals began with Gallup’s work (Gallup, 1970; Gallup, Anderson, & Shillito, 2002). Starting from the evidence that chimpanzees use mirrors to inspect their images, Gallup developed a protocol that allows an objective way to determine if they have a ToM. By anesthetizing his subjects and marking their foreheads with a dot, he observed what happened once awake, when they were able to saw themselves in the mirror. Results revealed that they touched their own foreheads in the region of the mark significantly more frequently than controls without the dot. Gallup’s protocol has been applied with other great apes and some monkey species, but only chimpanzees and orangutans consistently passed the test. According to Gallup (1998), passing the test means that animals within a particular species are self-aware and can infer the states of mind of other

10

individuals. Also, and more importantly, self-awareness, consciousness and mind would be an expression of the same underlying process, because organisms aware of themselves can use their experience to model the experience of others. Nonetheless, such results are still controversial; for example, there is evidence that gorillas’ failure on the mirror dot test could be referred to a lack of motivation rather than a deficit in cognitive abilities and, more precisely, ToM (Shumaker & Swartz, 2002). Another possible explanation lies in the fact that gorillas naturally avoid eye contact with other conspecifics; so a possible reason for their mirror-test failure is that they divert gaze from their reflection and thus never learn to recognize themselves (Gallup, 1998). Also, as described by Gallup, who has worked with primates, although during his experiments monkeys never showed self-recognition, they turn to him directly when they see his reflection in the mirror. Moreover, if we think of the case of humans, we develop ToM at only around 3 years old. However, as suggested by Tye (2016), nobody would claim that a younger child cannot feel pain because it is incapable of recognizing that state as painful.

The use of the mirror test allowed to conclude that at least some species are actually aware of themselves, but, more importantly, that such self-awareness could enable them to infer the mental states of others, to sympathize, empathize and attribute intent, emotions and meaning to others’ behaviors (Gallup, 1998). This implies that these higher capabilities are not exclusive prerogative of humans.

Other perspectives, however, open the range of empirical investigations potentially to all those beings that undergo experiences (Tye, 2016). Godfrey-Smith (2016) asserts that consciousness is one possible example of subjective experience, but not the only one. Moreover, he suggested that subjective experience it’s not matter of all or nothing, but it is distributed according to a continuum. Thus, pain can be freely explored in all its forms.

Another possible position is the agnostic one, asserting that there is no more reason to say that they have consciousness (and feel pain) than not. The idea is that we are not entitled to make conclusions about animals’ inner states. This position was used by one of its supporters, Marian Stamp Dawkins, biologist and animal researcher, for to the development of a novel theory of animal welfare (Dawkins, 2012).

Do non-human animals feel pain? Answers from physiology

11

Considering the impossibility of verbal testimony, previous research and practice on pain experience in animals adopted one of three main approaches: a) measuring of general body functioning (i.e. food and water intake, weight variations); b) measuring of physiological responses (i.e. cortisol concentrations to identify stress responses); c) measuring of behavioral patterns such as vocalizations, which falls more within an ethological perspective (Weary et al., 2006).

However, these measures can only provide a cue on specific variations within a time interval but cannot reflect the pain experience. Also, there are increasing difficulties in assessing pain, as well as cognitive and emotional abilities, as we get to species that are phylogenetically more and more distant from humans, and unfamiliar to our mammalian sensitivities (Allen, 2004). In these cases, in fact, the similarities are fewer and less evident, and confidence in our ability to assess pain is subsequently weaker.

Parallels between humans and animals

One possible solution to investigate animals’ pain is to explore the presence of similarities and differences in humans’ and animals’ physiology. In an attempt to formalize the requirements to assess conscious experience of pain in non-human animals, Varner (1998) has presented a table cross-tabulating six conditions with seven taxonomic groups including three invertebrates (earthworms, insects, and cephalopods) and four vertebrates (fish, herpetological fauna, birds, and mammals). The six conditions include: 1. the presence of nociceptors; 2. The presence of a central nervous system (CNS); 3. whether the nociceptors are connected to the CNS; 4. whether endogenous opioids are present; 5. whether analgesics affect responses; and 6. whether the behavioral responses are similar to those of humans. According to this model, only mammals fit all six conditions, although there is strong evidence of the presence of five of the six conditions in birds, where only condition 3 about the attachment of the nociceptors to the CNS is missing. Also, for what concerns condition 4 about the presence of endogenous opioids, Varner found evidence in all groups except for the cephalopods. Moreover, although the table indicates evidence for the presence of nociceptors only in mammals and birds, it has been found even in a marine snail and in frogs (Downes, Koop, Klopfenstein, & Lessov, 1999). It is also important to note, in general, that

12

the lack of evidence for any of these criteria does not prove its real absence. For what concerns criteria 1 to 5, describing anatomy and physiology domains, Varner’s results seem to highlight the presence of many similarities between species. Criteria 6, instead, referred to behavioral responses, lead to focus on particular behaviors like vocalization during pain, but also learnt responses, or responses to pharmacological interventions.

In a similar direction, Bermond (2001) distinguished between the perception of pain as a stimulus, which does not induce feelings of suffering and could thus be equated to nociception, and the experience of pain as an emotion, which, instead, is related to suffering and conscious pain experience. Bermond suggested that the first step occurs at the level of the spinal cord where the nature, intensity, location, and duration of noxious events are processed, and is considered more primitive, since it developed earlier in evolution. For what concerns emotional experience of pain, instead, the author posited the involvement of the prefrontal cortex (PFC) for the affective experience of pain. In fact, it has been demonstrated that an impairment in this area can lead to preserved pain perception, but absent emotional experience of pain. Thus, given that only humans and higher apes show a well-developed PFC, Bermond concluded that only these species have the capacity to suffer. Thus, this idea led to consider that pain in animals could be somehow close to the experience of lobotomized humans, who refer a noxious perception when pierced by a pin, but in the absence of subsequent agony or suffering (Anil, Anil, & Deen, 2002). They simply don’t care about it and show reduced emotional affect (Rowan, 1988).

However, in his recent book “Tense bees and shell-shocked crabs: Are animals conscious? (Tye, 2016), Tye makes three objections to this point. First, it has been shown that decorticate children can sometimes feel pain. Also, experiments on decorticated rats revealed that, if given normal developmental opportunities, they display very little impairment (Jaak Panksepp, Normansell, Cox, & Siviy, 1994). Finally, he claims that the absence of a neocortex doesn’t prevent the presence of homologous cells elsewhere. In fact, as suggested by Weary and colleagues (Weary et al., 2006), a possible rejoinder to these arguments is that similar functions are often subserved by different neural structures in different species. For example, Braithwaite and Huntingford (2004) described the case of visual systems in avian and mammalian, which, although supported by different pathways and neural correlates, can perceive and process the same type of information. Hence, it could also be possible that species lacking a well-

13

developed PFC may still experience harmful stimuli as unpleasant by using other brain networks.

Thus, it is necessary to look for the site of a specific function without assuming it will mirror a human’s area. Similarly, it is not prudent to conclude that a function is missing if the area is small as compared to humans’ one (Broom, 2001).

Indeed, there are many mechanisms that humans and non-human animals share in different ways. Let us consider pain receptors. As revealed by Ferdowsian (2012), in vertebrates pain is mediated by somatosensory neurons which terminate in the skin or other tissues. When a somatosensory stimulus is administered, it triggers electrical impulses that are interpreted by the brain. Intracellular recordings confirmed the presence of such mechanisms in lamprey (Martin & Wickelgren, 1971), with an output very similar to mammalian pain receptor. However, it has been proven that invertebrates also possess coordinated responses to painful stimulation, involving brain centers that organize even complex cognitive abilities such as memory, learning, and decision making.

Another point involves the effect of analgesics in modifying pain responses, that is shared by all vertebrates. For example, goldfish show a reaction similar to humans when subjected to difficult conditions (Denzer & Laudien, 1987).

Finally, pain involves a series of physiological reactions involving organ systems that are critical to disease progression and recovery (Gregory, 2004). At the same time, however, it is important to know that even if animals have the same nociceptors and nerve fibers which transmit pain in humans, this does not imply that they can experience unpleasant feelings of pain, because this kind of experience relies on the particular way information is processed in the brain. Similarly, the recording of physiological changes, such as increased heart rate, does not prove that the animal experiences pain, in that similar physiological modulations can occur unconsciously, or even in response to pleasant stimuli. That said, there are numerous similarities between animals and humans and that could be at least a starting point in the assessment of pain. In parallel to these attempts to theorize or conceptualize animals’ pain, some scientists focused on particular species of interest.

Fishes

A famous paper written by Key and entitled “Why fish do not feel pain” (Key, 2016) generated a flourishing debate about fishes’ abilities to

14

experience pain. According to Key’s point of view, fish cannot feel pain. His firm statement is based on inferences derived from experimental evidence from neuroscience and evolutionary biology investigations comparing humans and non-human animals and is based upon the certainty that fishes lack the specific neuroanatomical structures and neural circuits to perform the neural processing that are necessary for feeling pain. Key’s sharp point of view got other scientists to reply with different arguments.

Broom (2016), for example, asserts that recent information about fear and pain behaviors shows that fishes possess brain areas, like the lateral telencephalic pallium, that are very close in function to the amygdala and hippocampus in mammals, associated with emotion, feeling and learning from emotions (Portavella, 2004). A concrete example was provided by Muto and colleagues (Muto, Ohkura, Abe, Nakai, & Kawakami, 2013) who revealed that zebrafish, learning from a fear situation, shows brain activity in the habenula, while a transgenic fish that lacks such areas couldn’t respond to and learn from fear responses. Also, he asserted that Key’s argument about the effects of lesions on pallial sub-regions in fish does not show that it doesn’t feel pain. The findings of Portavella, in fact, strongly support the existence of systems for emotional response and learning from fear and pain in fish.

Many other similar examples are offered in Tye’s book (2016) such as Millsopp and Laming experiment (Millsopp & Laming, 2008). Here, the fish were trained to feed in a corner of an aquarium where they received a shock to the flank. Results showed that the number of feeding attempts decreased as shock intensity increased, unless they were starving. Thus, the authors concluded for the presence of a sort of negotiation of needs. In another experiment, Nordgreen and colleagues (Nordgreen et al., 2009) used two groups of goldfish. In the experimental group fishes were injected with morphine, while in the control group with saline. Then, water’s temperature was raised. Later, the group injected with morphine swam around as usual, while the control group showed defensive behaviors. The authors concluded that, without analgesia, fish “consciously perceive the situation as painful” and show stress-related behaviors. Moreover, it has been shown that pain can also affect motivation in fish. For example, trout injected with acetic acid in the lips took a long time to feed again (Sneddon, 2003). However, these examples are subject to many alternative interpretations directed towards more reductive positions.

Finally, Broom concludes that evidence of pain system function in fish is so similar to that of humans and other mammals, that it is not logical to

15

deduce that fish cannot feel pain. However, probably, more scientific data are needed to understand how fishes’ brain works, but the incompleteness of available knowledge suggests caution in inferring that they do not feel pain (Sneddon, 2016). It is also important to be careful to subjective moral motivations underlying such conclusions: in fact, according to Haikonen (2016), Key’s reasoning (2016) is based on his personal moral view in that it begins with a description of the problems that might arise for the fishing industry and the economy in general if it should be proved that fish can feel pain, which is very misleading.

Other species

Although less abundant, research on pain perception in birds also provided some intriguing results. For example, farm-raised chickens that become lame prefer food that contains a pain reliever over non-lame individuals. Also, the lamer the chicken, the greater its intake of drug added food (Danbury, Weeks, Waterman-Pearson, Kestin, & Chambers, 2000). Interestingly, there is also evidence of empathic responding towards others in pain in female chickens. For the experiment, mothers were forced to see the researchers blowing some air across their chicks’ feathers, thus causing them distress. Consequently, chickens reacted by mirroring distress and providing protective behaviors (Edgar, Lowe, Paul, & Nicol, 2011). Such findings have important implications for the treatment of chickens in cages that are forced to witness the distress of other individuals.

The case of invertebrates is much more controversial. In a series of experiments, Appel and Elwood (2009) provided hermit crabs with electric shock by rolling wires around their shells. The typical response after shocks is to abandon the shell. Then, they diminished the level of shock to a tolerable level, which made the hermit crabs to stay in their shell. Afterwards, they made available new shells. Results showed that only shocked hermit crabs checked the new shells out and abandon their old shells for the new ones, if compared to a control group of non-shocked hermit crab. According to Tye, the best explanation is that shocked hermit crabs remembered the painful experience delivered by the old shells, and preferred new shells that do not cause any pain (Tye, 2016).

Let us consider the case of bees. Although insect lack nociceptor, experimental evidence revealed that they respond to noxious or stressful stimulation by modifying their behavior. For example, in an early

16

experiment, bees’ stringing response was measured after being electrically shocked. Results showed that, after being injected with morphine, their stinging response diminished (Balderrama, Díaz, Sequeda, Núnez, & Maldonado, 1987) since they were not feeling as much pain from the shock, possibly.

Pain modulation

Weary and colleagues (Weary et al., 2006) point out another possible solution to assess pain in animals. It was already proposed by Gentle (2001), a neurophysiologist, who conducted an experimental study on pain in chickens. Starting from the idea that the human experience of pain can be modulated by shifting the patient’s attention elsewhere through different methods like relaxation or hypnosis, he explored the behavioral reactions to pain in chickens by redirecting their attention so that, if their reaction to a harmful event was simply a primitive, automatic reaction, then this operation should not influence their response. Otherwise, if they could experience pain by an emotional point of view, then redirecting their attention could reduce the signs of pain exactly like humans. Chickens received an injection of sodium urate crystals into one leg joint, that produce changes in behavior consistent with mild pain for about 3 hours. Usually, birds’ responses consist in removing weight on the affected leg and walking with a limp. However, results showed that these kinds of behavior were reduced or even eliminated if placing the bird into a pen with a novel feature or with an unfamiliar chicken, since they were distracted from perceived pain. Thus, the author concluded that, since the birds’ reaction to the injection was modified by shifting their attention elsewhere, the reaction must have been mediated by conscious awareness of pain and can no longer been explained as an unconscious adjustment of behavior.

These findings reinforce the idea of pain as a form of elementary and widespread subjective experience, present in animals with brains that are very different from ours (Godfrey-Smith, 2016).

Not forgetting the cumbersome moral concerns that such studies should address, in this way research was able to infer the animal’s experience by manipulating some experimental variables of interest and to observe directly how pain can modulate it.

Also, although research on the shared pain-related physiological correlates can provide meaningful evidence, it is much more important to go beyond these mechanisms and favor a deeper understanding of animals’

17

emotional life (Bekoff, 2006). In the following paragraph a new perspective will be presented. The possibility to infer the presence of a subjective dimension of pain will be highlighted by exploring animals’ comprehension of painful experience in others. In detail, complex emotional sharing, pain modulation during social interaction, empathy and sympathy will be considered.

Can animals perceive pain in others? A new perspective

Together with the main features of pain that have been described in the previous paragraphs about philosophical and physiological aspects, in recent times research on humans has brought attention to the importance of considering pain as a social phenomenon, an example of communication between conspecifics. This perspective falls into a more general approach: The biopsychosocial model of pain (Hadjistavropoulos et al., 2011; Lumley et al., 2011). Accordingly, even if we accepted a definition of pain as a private, subjective experience, there is also a shared dimension that can be considered. Research on human subjects already underlined the influence of emotions in modulating pain experience, the role of others’ and the mediation of empathy over pain perception (Lumley et al., 2011). Thus, we believe that the same considerations could be applied to the animal kingdom to expand the research and the observations on the subject. In fact, we believe that including animals’ empathic responses to other conspecifics in pain could provide a further clue about their attitude and understanding of pain experience.

But let’s make a step back. What do we mean with empathic responding? Empathy is usually defined as the ability to perceive, share, and understand others’ mental states and moods. This capacity is fundamental in that it reinforces and maintains our social bonds (Balconi & Vanutelli, 2017a; Vanutelli & Balconi, 2015a). Empathy, in fact, allows individuals to share the affective states of others, to predict their actions, and stimulate prosocial and helping behaviors (Balconi & Vanutelli, 2017b; Vanutelli & Balconi, 2015a; Vanutelli, Nandrino, & Balconi, 2016). Thus, empathy and altruism are commonly considered forms of compassion that human beings express toward one another. What is not clear, however, is the extent to which non-human animals can perceive others’ feelings and empathize with them (Vanutelli & Balconi, 2015a).

18

The influential work of de Waal (2008) and Preston and de Waal (Preston & de Waal, 2002a) contributed to the idea that empathy could be a phylogenetically continuous ability, ranging across animals with simpler and automatic reactions in response to the emotions of others, till perspective-taking. The authors, in fact, proposed a sequence of progressively complex levels of empathy across animals that parallels the development of empathy in humans.

Also, Gonzales-Liencres and colleagues (Gonzalez-Liencres, Shamay-Tsoory, & Brüne, 2013) proposed a phylogenetic hierarchy of empathy-related capacities to explore the boundaries of empathy, starting with the simplest forms and leading up to compassion. Mimicry has been defined as an automatic process by which an individual mimics another’s motor actions, among which vocalizations, facial expressions, posture and gestures (Singer & Lamm, 2009). We share this kind of behavior with mammals, but also with birds and other vertebrates (Zentall, 2004). With the term emotional contagion, instead, they referred to a copy of a behavior which is generated by observing and perceiving the emotions that another individual is expressing (Balconi & Vanutelli, 2015). This fact account for a higher position of emotional contagion with respect to mimicry which, instead, doesn’t need the presence of emotions. These two competencies could be actually considered the precursors of empathy. Proceeding in complexity we find imitation, which involves an intentional act aiming at achieving the same observed goal. Imitation does not necessarily involve a corresponding emotion between the two actors. Emotional empathy comes next: it requires self/other distinction (Singer & Lamm, 2009), which is not a prerequisite for the previous competencies, such as mimicry or emotional contagion. Emotional empathy implies to feel what another person is feeling, or, in the case of cognitive empathy, knowing his mental states (Balconi & Bortolotti, 2012). Thus, emotional empathy implies an embodied representation of the mental state of another individual, and, at the same time, of being aware of the cause of the other’s emotional state (Vanutelli & Balconi, 2015b). Furthermore, authors describe sympathy, which leads to helping behavior in order to alleviate the distress of others. The last step is compassion, defined as a feeling that involves empathic concern for others and induces caring or comforting behaviors (Goetz, Keltner, & Simon-Thomas, 2010; Singer & Lamm, 2009). Compassion does not necessary imply sharing feelings.

As already suggested by de Waal (2008), this broad perspective on empathy suggests a continuity between humans and other animals. In this

19

perspective, affective behaviors in response to emotion of others are rather common in animals (Preston & de Waal, 2002b).

Ethological observations

Darwin himself already noted that “many animals certainly sympathize with each other’s distress or danger (Darwin, 1982 [1871], p. 77)” and display grief at the loss of a close friend. For example, consolation behaviors have been analyzed in non-human primates as an evidence of sympathetic concern. It has been shown that, after a fight, a third party intervenes going towards the loser and embrace an arm around his shoulders. De Waal & van Roosmalen (1979) and de Waal & Aureli (1996)also showed that bystanders support victims of aggression more often than they contact aggressors, especially when the victims receives serious aggressions with regard to those who had received mild aggression.

Similarly, Konrad Lorenz reported grief-related behaviors in geese that he described as similar to those in young children (Lorenz, 1991). Other ethological observations are offered by Bekoff (2000, 2006). For example, he described how sea lion mothers, while watching their babies being eaten by killer whales, scream as they are lamenting their loss. Dolphins have also been found to struggle in the attempt to save a dead infant.

One of the best example of shared pain-related behaviors within the animal kingdom is that of elephants: as described by Bates and colleagues (Bates et al., 2008), elephants show a rich social organization, which includes coalition formation, the offering of protection and comfort to others, retrieving and babysitting calves, aiding individuals in difficulty, and removing foreign objects attached to others. Also, it has been observed that they show interest in the carcasses and bones of dead conspecifics, which might be viewed as evidence of their empathic concern, although the biological functions of these behaviors are still unclear (Douglas-Hamilton, Bhalla, Wittemyer, & Vollrath, 2006; McComb, Baker, & Moss, 2006). Also, some assisting behaviors has been recorded, like helping others that are injured, extracting tranquilizing darts from their companions, or even spraying dust on others’ wounds. The presence of such behaviors demonstrates that an elephant is capable of diagnosing animacy and goal directedness, and is able to understand the physical competence, emotional state and intentions of others, even if different from its own (Bates et al., 2008). Moreover, elephants have been observed to stand guard over a stillborn baby for days showing depressive behaviors (Bekoff, 2006).

20

Indeed, grief and depression among orphan elephant babies have been consistently reported (Bekoff, 2000; Poole, 1998).

Finally, considering domesticated species that are more familiar to our daily experience, an interesting study exploring children’s emotional behaviors in response to family members instructed to feign sadness (sobbing), pain (crying), or distress (choking), highlighted striking similarities between the reactions of one-year-old children and pets, such as cats and dogs. The latter, in fact, showed comforting attempts as well, such as putting their head in the lap of the complaining person (Zahn-Waxler, Hollenbeck, & Radke-Yarrow, 1984).

Laboratory studies

Much of the existent knowledge about emotional and social factors related to pain comes from laboratory studies. Even earlier work, for example, showed that rats and pigeons display distress when perceiving distress in a conspecific, and interrupt conditioned behavior if it can cause painful responses to others (Church, 1959; Watanabe & Ono, 1986). The most pioneering and systematic studies in this field were made with non-human primates. Wechkin and colleagues (1964) and Masserman and colleagues (1964) found that monkeys refuse to pull a chain that delivers food when realizing that, doing so, another companion receives an electric shock causing pain reactions.

One other interesting case is that of mice: as already described by Vanutelli and Balconi (2015), a research line by Langford and colleagues (2006) explored the experience of pain in mice from a social point of view, in the attempt to demonstrate their prosocial and empathic competencies. They reported the modulation of pain sensitivity in mice induced by exposure to their cage mates in pain. The experiments were conducted by placing pairs of mice in two transparent Plexiglas cylinders in a way that they could see each other, and were injected with acetic acid, which is known to produce a mild stomachache and characteristic stretching movements. Results revealed that an injected mouse showed intensified pain behaviors if its partner displayed the same behavior. Also, the effect was strengthened for mouse pairs who have also been cage mates, if compared to stranger individuals. Finally, Langford and colleagues (Langford et al., 2009) reported that female mice placed in an alley containing trapped cage mate mice at both ends spent more time in close

21

proximity to the jailed mouse in pain. The provided proximity positively influenced the perceived pain in the jailed subject, suggesting that the approach behavior produced analgesia. Thus, these experiments showed that rodents can recognize and show emotional reactions to the pain of conspecifics, and that their pain sensitivity can be altered by social factors. A further result of interest revealed that a mouse in pain show a pattern of synchronized behaviors with another mice in pain significantly higher than chance and compared to control mice. Such finding is noteworthy since a similar mechanism is present also in humans during meaningful empathic social exchange (Ham & Tronick, 2009; Reed, Randall, Post, & Butler, 2013; Smith et al., 2011; Vanutelli et al., 2016; Vanutelli, Gatti, Angioletti, & Balconi, 2017).

Moreover, Norman and colleagues (Norman et al., 2010) found that social interaction can prevent the onset of depressive behavior after lesion in mice. After being either paired housed or individually housed, mice underwent nerve injury surgery. Then, only isolated individuals developed depressive-like behaviors as assessed by an increased expression of a molecule, interleukin-1β, within the frontal cortex.

As also reported by Panksepp & Panksepp (2013), both rats (Atsak et al., 2011; Kim, Kim, Covey, & Kim, 2010; Wöhr & Schwarting, 2008) and mice (Jeon et al., 2010) express increased freezing behaviors when distress is induced in social partners, highlighting the emotional contagion of fear. What is more interesting is that this kind of social interactions mediating pain can prime rodents for subsequent learning. In fact it has been shown that social experiences with frightened partners can retard (Bredy & Barad, 2009) and enhance (Knapska, Mikosz, Werka, & Maren, 2009) consequent acquisitions of fearful memories in mice and rats.

Such evidence arises some important highlights on complex experience of pain in mice, which should lead to improve available knowledge on animal pain.

Insights from ethology

When trying to highlight the presence of a subjective dimension of pain in non-human animals and analyzing the differences and similarities between pain-related behaviors and physiological mechanisms in human

22

and non-human animals, we must also keep in mind the ethological aspects of each species. In fact, although we know very well the human repertoire involving facial expressions, bodily postures, vocalization, behaviors and social sharing of pain in humans, we are not so good at recognizing signs of pain experience in other species, especially for those that are phylogenetically more distant from us or, more simply, less familiar.

Highly social species such as humans or dogs, live in groups with other individuals. Thus, it may beneficial for them to share their pain experience. In fact, establishing a communication about pain experience could be beneficial for both the receiver and the sender. The receiver is warned about potential danger and can improve the ability to identify and understand others’ feelings, while the sender can induce help mechanisms in the other (Mogil, 2015). Apparently, this vision seems rather simplistic. Let us take the example of prosocial behaviors. It has been shown that they evolved for utilitarian reasons, such as to reinforce group dynamics and be reciprocated (Vanutelli et al., 2016). However, the social exchange became inherently rewarding in humans. We could hypothesize a similar pathway for at least some animal species.

Conversely, those species considered as prey animals are used to suppress their pain-related behaviors, such as vocalization, grimacing or writhing. For example, Broom (2001) reports the example of African antelopes or sheeps, which are extremely exposed to predators’ attacks. Since predators usually attack weaker individuals, vocalizations would result in a death sentence. Thus, these species do not vocalize when injured. That’s why, for example, sheeps do not emit sounds when they undergo Mulesing operation in farms, thus leading farmers to conclude that they don’t feel pain. The truth is that, after this mutilation, they show other reactions, such as cortisol and β-endorphin release (Shutt et al., 1987). The same applies to monkeys giving birth, which are at increased risk from predators.

Thus, the evolutionary history and species-specific features of animals’ behavior could be of great importance in avoiding both reductionistic and anthropomorphic views. Also, a deep knowledge of the evolutionary and selective pressures on each species is necessary for a complete and truthful interpretation of pain-related behaviors (Broom, 2001).

Legal and ethical matters

23

As pointed out by Bateson (1991) people differ a lot in defining whether animals feel pain, to what extent, and in the efforts they punt into stop potentially painful practices. The discussion argued above concluded for the presence of some kind of pain experience also in non-human animals, which could take us towards at least an agnostic position. In fact, because of the complexity of the topic, animals should deserve the benefit of the doubt. However, given this evidence, how we should deal with animals’ pain?

Tye’s position (2016) recommend that, given the similarities in our bodily and emotional experiences, we should behave towards them as we would do towards other human beings. However, the author also introduces an important construct, that is speciesism. In his book “Tense bees and shell-shocked crabs” he proposes some moral dilemmas involving whether to save a human at the expense of other (although many) animal beings. Tye highlights how, although aware of the significant emotional and subjective experience of animals, we tend to favor the members of our own species. Nonetheless, he concludes that speciesism should not justify an unequal or unrespectful treatment over other species.

Another interesting point of view was raised by Mroczek (1992) and referred to the importance to pay attention to animals as subjects, in the sense of individual creatures, and as members of a species involving a prototypical set of psychobiological features. The recognition of a subjective dimension requires the involvement of empathy and compassion, while the species-specific definition needs observation and a deep knowledge of instincts, biological patterns, motivations and aims, as reported just above.

However, it seems that, when dealing with animals’ suffering, there is something more that goes beyond the scientific available evidence about philosophical, ethological and neuroscientific issues. In fact, many other personal dimensions must be considered, such as ethical and moral values, which are, of course, even more difficult to address. For example, people who care deeply about animals may not be interested in all that information concerning pain assessment. In fact, they could believe that, whether in pain or not, it is not humans’ business to decide upon animals’ lives. Similarly, a speciesist individual will always favor humans’ wellbeing irrespective of any other animal’s right. Of course, many other intermediate levels are contemplated. Accordingly, “moral and ethical issues are not ones that play a large part in the specific moral concern that underlies the

24

need for assessments of pain” (Bateson, 1991, p. 837). In fact, it applies more to the cases in which higher standards of welfare are desired.

The focus on each particular species is very important when considering animal welfare protections. In fact, they should cover a complete range of species to develop species-specific measures of pain with the aim to develop a more humane relationship with animals. For example, as revealed by the described studies on fish pain, the anatomy, physiology and behavior of fish suggest, according to Chandroo and colleagues (Chandroo, Duncan, & Moccia, 2004), that they are more likely to be sentient than not. Therefore, thinking about fish farming enterprise, the welfare of fishes requires consideration. In fact, starting from the idea that animals have the capacity to suffer, therefore their quality of life is greatly determined by how much it may suffer under captive conditions (Duncan & Fraser, 1997).

Godfrey-Smith (2016), in his eminent book “Other minds: The octopus and the evolution of intelligent life” describes the use of octopus in laboratory experiments. He explains how, being invertebrates, these animals were at first treated very badly and without any protection. However, in the last decade, they became to be more protected and upgraded in the legislation, almost as if they were “honorary vertebrates” (p. 75). Thus, welfare policies should be appropriate for the affective and cognitive abilities that target animals may possess.

For example, considering the current policies of the U. S. Department of Agriculture, a painful procedure is still defined by an anthropocentric point of view and described as “any procedure that would reasonably be expected to cause more than slight or momentary pain or distress in a human being to which that procedure was applied” (Allen, 2004). Nonetheless, this definition is weak in that it can lead to mistakes in a double way: in fact, there are procedures that do not cause pain in humans, but might cause pain in animals, like ultrasounds. In parallel, procedures perceived as painful by humans like walking barefoot across a very hot floor could not be experienced as painful by species that live in the desert (Allen, 2004). Knowing what can be perceived as painful by other species could help us to “do our best to minimize these negative mental states in our treatment of them (Tye, 2016, p. 209).

We would like to conclude this section by illustrating a new point of view about the widespread distinction between “lower” and “higher” pain mechanisms in relation to animals and humans, respectively. In fact, the common view assumes that the greater cognitive abilities of humans could

25

lead to heavier pain experiences. However, Broom offers a new, opposite perspective, where greater cognitive abilities would, instead, result in greater coping abilities and a better management of pain. It follows that pain experience could be worse in animals with poorer cognitive abilities which can’t rationalize it (Broom, 2001). Accordingly, humans should make an even greater effort to minimize animals’ pain, by being compassionate and empathizing with them.

Conclusions

The present study aimed at reviewing the most eminent evidence about pain experience in humans and non-human animals, to explore continuities and specificities within a comparative perspective.

The first issue to consider is that conventional behavioral indices to attest human consciousness could not be applied to other species, since it is based on verbal indices, thus raising the need for alternative ways to assess non-human animals’ painful experience. In fact, due probably to this criticality, a distinction between two different forms of pain has been conventionally proposed, with one being a non-conscious neural processing of stimuli shared by humans and most of non-human animals, and a second one related to higher-levels pain experiences, shared only between humans and great apes. Nonetheless, more recent perspectives consider this distinction as old-fashioned, as well as misleading in that it creates an artificial boundary between humans and other animals, or between "higher" and "lower" animals (Broom, 2016).

Considering the philosophical point of view, two different positions are conventionally taken: those who think that the similarities between humans and other non-human animals lead directly to think that animals experience pain consciously, and those who think that animals can’t experience pain consciously at all. Being both affected by theoretical bias, more recent attempts tried to support the presence of self-awareness and ToM in animals by more objective paradigms based on ethological observations. Such studies allowed to conclude that some species are actually aware of themselves, but, more importantly, that such self-awareness could enable them to infer the mental states of others, to sympathize, empathize and attribute intent, emotions and meaning to others’ behaviors (Gallup, 1998).

26

However, other perspectives suggested to embrace a wider definition of consciousness to include all kinds of pain experience in non-human animals (Godfrey-Smith, 2016). In this case, the focus is the subjective experience, as a mean to explore pain freely in all its forms. Also, when we face behaviors that can be interpreted as pain-related experiences in animals, the simpler hypothesis that we share similar feelings should be preferred, until proven otherwise.

Another possible position is the agnostic one, asserting that there is no more reason to say that animals have consciousness (and feel pain) than not. The underlying principle is that we are not entitled to make conclusions about animals’ inner states. Although cautions, the adoption of such view can anyhow lead to the adoption of forms of protection in favor of non-human animals.

Evidence from physiology revealed that perception of noxious stimuli occurs at the level of the spinal cord, while emotional experience of pain is assigned to the PFC, which is associated with affective evaluation of stimuli, subjective experience and self-reflection (Hecht, Patterson, & Barbey, 2012). Subsequently, only humans and great apes should thus be capable of conscious painful experiences. Nonetheless these arguments could be weak if considering, for example, that similar functions could be often served by different neural structures in different species, and that the absence of a neocortex does not necessary lead to a complete impairment is consciousness or pain experience. Thus, it could be possible that species without neocortex may have developed other brain networks in a way to experience conscious pain. There are many pain-related mechanisms that we share with animals, even if the underlying networks lie in different structures. We can mention the effects of analgesics in modifying pain, the presence of physiological reactions, and the capacity of brain centers to organize complex cognitive abilities such as memory, learning, and decision making in response to noxious stimulation.

In parallel, it is also important to note that the presence of comparable neural structures in humans and non-human animals, such as nociceptors and nerve fibers, does not imply that they can experience the same feelings in that what is important is how information is processed in the brain.

27

A possible solution to such critical points, and also an interesting way to identify pain knowledge in animals, is to explore how pain can modulate the animal’s experience and behavior in a way to distinguish unconscious adjustments of behavior from conscious awareness of pain. In particular, it should be possible to observe how the animal’s experience of pain can be modulated by different cognitive and affective intervening conditions, to explore changes in goals, intentions and behaviors, thus inferring the presence of any kind of subjectivity.

In the present work, available evidence of such examples of complex emotional sharing within the animal kingdom, like pain modulation during social interaction, empathy and sympathy, have been highlighted as a further tool to assess animacy, goal directedness, and other emotional and affective competencies towards the understanding of pain in others and, subsequently, the presence of conscious and reflective experience of pain. These studies mostly focused on non-human primates but demonstrated complex social management of pain also in mice and rats, elephants, dogs and cats. Unfortunately, these considerations remain circumscribed to the case of social species.

Moreover, some caveats have been proposed from ethology. In fact, when trying to assess the presence of a subjective dimension of pain in non-human animals it is extremely important to know the evolutionary history and the selective pressures on each species for a complete and truthful interpretation of pain-related behaviors. For example, the absence of vocalization in prey animals undergoing noxious stimulation must not be interpreted as they do not feel pain, but rather framed according to their evolutionary need to protect from predators and be discreet. A completely different situation is that of highly social species who benefit from signaling danger and pain to other members of the group.

Finally, some ethical and moral issues related to animals’ treatment have been provided with respect to humans’ attitude to animals’ pain. In fact, the presence of scientific evidence doesn’t seem sufficient to define people position towards the topic. In fact, many personal issues, such as moral and ethical positions, influence our attitudes to scientific and philosophical perspectives, such as speciesism or animalism. However, it is anyhow significant that evidence on animals’ pain are shared and applied to welfare protections and farming policies. In fact, it should be important to pay attention to animals as individual creatures, and as member of a species to respect their prototypical set of psychobiological features and develop a more humane relationship with them. Knowing what can be perceived as

28

painful by other species could help us to “do our best to minimize these negative mental states in our treatment of them (Tye, 2016, p. 209). Starting from here, more research is needed to show emotion and pain processing, as well as consciousness, in non-human animals, trying to avoid both anthropocentric and anthropodenial points of view.

According to the evidence discussed in the paper, we believe that it is unlikely that consciousness and pain experience appeared suddenly in humans in their “final” form. Rather, we think that it is more reasonable to assume that they evolved and changed in time from simpler to more complex forms that deserve our interest and scientific commitment (see also Godfrey-Smith, 2016).

The present work does not pretend to be exhaustive in all its sections, nor conclusive in its arguments, but it offers some insights about the debate on pain experience in animals, which could attract the attention of the scientific world for future research, with a specific interest for the ethological and neuroscientific contribution.

29

Acknowledgements

None

Funding

None

30

References

Aitken, G. (2008). Animal Suffering : An Evolutionary Approach. Environmental Values, 17, 165–180. https://doi.org/10.3197/096327108X303837

Allen, C. (2004). Animal pain. Noûs, 38(4), 617–643. https://doi.org/10.1111/j.0029-4624.2004.00486.x

Anil, S. S., Anil, L., & Deen, J. (2002). Challenges of pain assessment in domestic animals. Journal of the American Veterinary Medical Association, 220(3), 313–319. https://doi.org/https://doi.org/10.2460/javma.2002.220.313

Appel, M., & Elwood, R. W. (2009). Motivational trade-offs and potential pain experience in hermit crabs. Applied Animal Behaviour Science, 119(1–2), 120–124. https://doi.org/10.1016/j.applanim.2009.03.013

Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., … Keysers, C. (2011). Experience modulates vicarious freezing in rats: A model for empathy. PLoS ONE, 6(7), e21855. https://doi.org/10.1371/journal.pone.0021855

Balconi, M., & Bortolotti, A. (2012). Empathy in cooperative versus non-cooperative situations: The contribution of self-report measures and autonomic responses. Applied Psychophysiology Biofeedback, 37(3), 161–169. https://doi.org/10.1007/s10484-012-9188-z

Balconi, M., & Vanutelli, M. E. (2015). Emotions and BIS/BAS components affect brain activity (ERPs and fNIRS) in observing intra-species and inter-species interactions. Brain Imaging and Behavior. https://doi.org/10.1007/s11682-015-9443-z

Balconi, M., & Vanutelli, M. E. (2017a). Empathy in negative and positive interpersonal interactions. What is the relationship between central (EEG, fNIRS) and peripheral (autonomic) neurophysiological responses? Advances in Cognitive Psychology, 13(1), 105–120. https://doi.org/10.5709/acp-0211-0

Balconi, M., & Vanutelli, M. E. (2017b). When cooperation was efficient or inefficient. Functional Near-Infrared Spectroscopy evidence. Frontiers in Systems Neuroscience, 11, 26. https://doi.org/10.3389/fnsys.2017.00026

Balderrama, N., Díaz, H., Sequeda, A., Núnez, J., and Maldonado, H. (1987). Behavioral and pharmacological analysis of the stinging response in africanized and italian bees. In R. Menzel & A. Mercer (Eds.), Neurobiology and Behavior of Honeybees (pp. 121– 128). New York: Springer- Verlag.

Bates, L. A., Lee, P. C., Njiraini, N., Poole, J. H., Sayialel, K., Sayialel, S.,

31

… Byrne, R. W. (2008). Do elephants show empathy? Journal of Consciousness Studies, 15(10–11), 204–225.

Bateson, P. (1991). Assessment of pain in animals. Animal Behaviour, 42(5), 827–839. https://doi.org/https://doi.org/10.1016/S0003-3472(05)80127-7

Bekoff, M. (2000). The smile of a dolphin: Remarkable accounts of animal emotions. New York: Random House/Discovery Books.

Bekoff, M. (2006). Animal Emotions: Exploring Passionate Natures. BioScience, 50(10), 861–870. https://doi.org/10.1641/0006-3568(2000)050[0861:aeepn]2.0.co;2

Bermond, B. (2001). A neuropsychological and evolutionary approach to animal consciousness and animal suffering. Animal Welfare, 10, S47–S62.

Boly, M., Garrido, M. I., Gosseries, O., Bruno, M., Laureys, S., & Friston, K. (2011). Preserved feedforward but impaired top-down processes in the vegetative state. Science, 332, 858–862. https://doi.org/10.1126/science.1202043

Braithwaite, V. A., & Huntingford, F. A. (2004). Fish and welfare: Do fish have the capacity for pain perception and suffering? Animal Welfare, 13, S87–S92.

Bredy, T. W., & Barad, M. (2009). Social modulation of associative fear learning by pheromone communication. Learning & Memory, 16(1), 12–18. https://doi.org/10.1101/lm.1226009

Bromm, B., & Lorenz, J. (1998). Neurophysiological evaluation of pain. Electroencephalography and Clinical Neurophysiology, 107, 227–253. https://doi.org/10.1016/S0013-4694(98)00075-3

Broom, D. M. (2001). The evolution of pain. Vlaams Diergeneeskundig Tijdschrift, 70(1), 17–21.

Broom, D. M. (2014). Sentience and Animal Welfare. Wallingford: CABI.Broom, D. M. (2016). Fish Brains and Behaviour Indicate Capacity for

Feeling Pain. Animal Sentience, 10(Commentary on Key on Fish Pain), 1–6.

Cabanac, M., Cabanac, A. J., & Parent, A. (2009). The emergence of consciousness in phylogeny. Behavioural Brain Research, 198(2), 267–272. https://doi.org/10.1016/j.bbr.2008.11.028

Carruthers, P. (2000). Phenomenal Consciousness. Cambridge: Cambridge University Press.

Chandroo, K. P., Duncan, I. J. H., & Moccia, R. D. (2004). Can fish suffer?: Perspectives on sentience, pain, fear and stress. Applied Animal Behaviour Science, 86(3–4), 225–250. https://doi.org/10.1016/j.applanim.2004.02.004

32

Changeux, J.-P. (2012). Conscious processing: implications for general anesthesia. Current Opinion in Anesthesiology, 25, 398–404. https://doi.org/10.1097/ACO.0b013e32835561de

Chapman, C. R. (1992). Suffering in animals: towards comprehensive definition and measurement for animal care. In T. R. Kuchel, M. Rose, & J. Burrell (Eds.), Animal Pain Ethical and Scientific Perspectives (pp. 19–25). Australian and New Zealand Council for the Care of Animals in Research and Teaching.

Church, R. M. (1959). Emotional reactions of rats to the pain of others. Journal of Comparative and Physiological Psychology, 52(2), 132–134. https://doi.org/10.1037/h0043531

Constant, I., & Sabourdin, N. (2015). Monitoring depth of anesthesia: from consciousness to nociception. A window on subcortical brain activity. Paediatric Anaesthesia, 25(1), 73–82. https://doi.org/10.1111/pan.12586

Danbury, T. C., Weeks, C. A., Waterman-Pearson, A. E., Kestin, S. C., & Chambers, J. P. (2000). Self-selection of the analgesic drug carprofen by lame broiler chickens. Veterinary Record, 146(11), 307–311. https://doi.org/10.1136/vr.146.11.307

Darwin, C. (1982). The Descent of Man, and Selection in Relation to Sex. Princeton: Princeton University Press.

Dawkins, M. S. (2012). Why animals matter: Animal consciousness, animal welfare, and human well-being. New York: Oxford University Press.

de Waal, F. B. M. (1997). Are we in anthropodenial? Discover, 18(7), 50–53.

de Waal, F. B. M. (2008). Putting the altruism back into altruism: the evolution of empathy. Annual Review of Psychology, 59, 279–300. https://doi.org/10.1146/annurev.psych.59.103006.093625

de Waal, F. B. M., & Aureli, F. (1996). Consolation, reconciliation, and a possible cognitive difference between macaque and chimpanzee. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into Thought: The Minds of the Great Apes (pp. 80–110). Cambridge: Cambridge University Press.

de Waal, F. B. M., & van Roosmalen, A. (1979). Reconciliation and consolation among chimpanzees. Behavioral Ecology and Sociobiology, (5), 55–66. https://doi.org/10.1007/BF00302695

Denzer, D., & Laudien, H. (1987). Stress induced biosynthesis of a 31 kd-glycoprotein in goldfish brain. Comparative Biochemistry and Physiology. B, Comparative Biochemistry, 86(3), 555–559. https://doi.org/10.1016/0305-0491(87)90447-0

Douglas-Hamilton, I., Bhalla, S., Wittemyer, G., & Vollrath, F. (2006).

33

Behavioural reactions of elephants towards a dying and deceased matriarch. Applied Animal Behaviour Science, 100(1–2), 87–102. https://doi.org/10.1016/j.applanim.2006.04.014

Downes, H., Koop, D. R., Klopfenstein, B., & Lessov, N. (1999). Retention of nociceptor responses during deep barbiturate anesthesia in frogs. Comparative Biochemistry and Physiology Part C: Pharmacology Toxicology and Endocrinology, 124(2), 203–210. https://doi.org/10.1016/S0742-8413(99)00069-9

Duncan, I. J. H., & Fraser, D. (1997). Understanding animal welfare. In M. C. Appleby & B. O. Hughes (Eds.), Animal Welfare, CAB International (pp. 19–31). Cambridge: University Press.

Edgar, J. L., Lowe, J. C., Paul, E. S., & Nicol, C. J. (2011). Avian maternal response to chick distress. Proceedings of the Royal Society B: Biological Sciences, 278(1721), 3129–3134. https://doi.org/10.1098/rspb.2010.2701

Elwood, R. W. (2018). Pain and suffering in invertebrates? ILAR Journal, 52(2), 175–184. https://doi.org/10.1093/ilar.52.2.175

Ferdowsian, H. (2012). Parallels in sources of trauma, pain, distress, and suffering in humans and nonhuman animals, 13(4), 448–468. https://doi.org/10.1080/15299732.2011.652346

Gallup, G. G. J. (1970). Chimpanzees: Self-recognition. Science, 167, 86–87. https://doi.org/10.1126/science.167.3914.86

Gallup, G. G. J. (1998). Can animals empathize? Yes. Scientific American, 9, 66–71.

Gallup, G. G. J., Anderson, J. R., & Shillito, D. J. (2002). The Mirror Test. In M. Bekoff, C. Allen, & G. M. Burghardt (Eds.), The Cognitive Animal (pp. 325–334). Cambridge: MIT Press.

Garcia-Larrea, L., Charles, N., Sindou, M., & Mauguiere, F. (1993). Flexion reflexes following anterolateral cordotomy in man: dissociation between pain sensation and nociceptive reflex RIII. Pain, 139, 149. https://doi.org/10.1016/0304-3959(93)90143-D

Gentle, M. J. (2001). Attentional shifts alter pain perception in the chicken. Animal Welfare, 10, S187–S194.

Godfrey-Smith, P. (2016). Other minds: The octopus and the evolution of intelligent life. London: William Collins.

Goetz, J. L., Keltner, D., & Simon-Thomas, E. (2010). Compassion: an evolutionary analysis and empirical review. Psychological Bulletin, 136, 351–374. https://doi.org/10.1037/a0018807

Gonzalez-Liencres, C., Shamay-Tsoory, S. G., & Brüne, M. (2013). Towards a neuroscience of empathy: Ontogeny, phylogeny, brain mechanisms, context and psychopathology. Neuroscience &

34

Biobehavioral Reviews, 37(8), 1537–1548. https://doi.org/10.1016/j.neubiorev.2013.05.001

Gregory, N. C. (2004). Physiology and behaviour of animal suffering. New York: Wiley.

Hadjistavropoulos, T., Craig, K. D., Duck, S., Cano, A., Goubert, L., Jackson, P. L., … Williams, A. C. de C. (2011). A biopsychosocial formulation of pain communication. Psychological Bulletin, 137(6), 910. https://doi.org/10.1037/a0023876

Haikonen, P. O. (2016). On the sentience of fish. Animal Sentience Haikonen Commentary on Key on Fish Pain, 10(Commentary on Key on Fish Pain), 1–2.

Ham, J., & Tronick, E. (2009). Relational psychophysiology: lessons from mother-infant physiology research on dyadically expanded states of consciousness. Psychotherapy Research : Journal of the Society for Psychotherapy Research, 19(6), 619–632. https://doi.org/10.1080/10503300802609672

Hecht, E. E., Patterson, R., & Barbey, A. K. (2012). What can other animals tell us about human social cognition? An evolutionary perspective on reflective and reflexive processing. Frontiers in Human Neuroscience, 6, 1–13. https://doi.org/10.3389/fnhum.2012.00224

IASP. (1979). Pain terms: A list with definitions and notes on usage. Pain, 6, 247–252.

Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., … Shin, H.-S. (2010). Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nature Neuroscience, 13(4), 482–8. https://doi.org/10.1038/nn.2504

Key, B. (2016). Why fish do not feel pain. Animal Sentience, 3(Key on Fish Pain), 1–33.

Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010). Social transmission of fear in rats: The role of 22-kHz ultrasonic distress vocalization. PLoS ONE, 5(12), e15077. https://doi.org/10.1371/journal.pone.0015077

Knapska, E., Mikosz, M., Werka, T., & Maren, S. (2009). Social modulation of learning in rats. Learning and Memory, 17, 35–42. https://doi.org/10.1101/lm.1670910

Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., … Mogil, J. S. (2006). Social modulation of pain as evidence for empathy in mice. Science, 312(5782), 1967–1970. https://doi.org/10.1126/science.1128322

Langford, D. J., Tuttle, A. H., Brown, K., Deschenes, S., Fischer, D. B.,

35

Mutso, A., … Sternberg, W. F. (2009). Social approach to pain in laboratory mice. Social Neuroscience, 5, 163–170. https://doi.org/10.1080/17470910903216609

Lorenz, K. Z. (1991). Here I Am-Where Are You? New York: Harcourt Brace Jovanovich.

Low, P. (2013). The Cambridge Declaration on Consciousness. In J. Panksepp, D. Ross, D. Edelman, B. Van Swinderen, & C. Koch (Eds.). Francis Crick Memorial Conference, University of Cambridge. 19th November 2012. https://doi.org/http://fcmconference.org/img/CambridgeDeclarationOnConsciousness.pdf

Lumley, M. A., Cohen, J. L., Borszcz, G. S., Cano, A., Radcliffe, A. M., Porter, L. S., … Keefe, F. J. (2011). Pain and emotion: A biopsychosocial review of recent research. Journal of Clinical Psychology, 67(9), 942–968. https://doi.org/10.1002/jclp.20816

Martin, A. R., & Wickelgren, W. O. (1971). Sensory cells in the spinal cord of the sea lamprey. The Journal of Physiology, 212(1), 65–83. https://doi.org/10.1113/jphysiol.1971.sp009310

Masserman, J., Wechkin, M. S., & Terris, W. (1964). Altruistic behavior in rhesus monkeys. The American Journal of Psychiatry, 121, 584–585. https://doi.org/10.1176/ajp.121.6.584

McComb, K., Baker, L., & Moss, C. (2006). African elephants show high levels of interest in the skulls and ivory of their own species. Biology Letters, 2(1), 26–28. https://doi.org/10.1098/rsbl.2005.0400

Millsopp, S., & Laming, P. (2008). Trade-offs between feeding and shock avoidance in goldfish (Carassius auratus). Applied Animal Behaviour Science, 113(1–3), 247–254. https://doi.org/10.1016/j.applanim.2007.11.004

Mogil, J. S. (2015). Social modulation of and by pain in humans and rodents. Pain, 156(4), S35–S41. https://doi.org/10.1097/01.j.pain.0000460341.62094.77

Mroczek, N. S. (1992). Point of view: Recognizing animal suffering and pain. Lab Animal, 21(9), 27–30.

Muto, A., Ohkura, M., Abe, G., Nakai, J., & Kawakami, K. (2013). Real-time visualization of neuronal activity during perception. Current Biology, 23(4), 307–311. https://doi.org/10.1016/j.cub.2012.12.040

National Research Council (US) Committee on recognition and alleviation of pain in laboratory animals. (2009). Pain in research animals: General principles and considerations. In Recognition and Alleviation of Pain in Laboratory Animals (National A, p. 1). Washington (DC).

Nelkin, N. (1986). Pains and pain sensation. The Journal of Philosophy,

36

83(3), 129–148. https://doi.org/10.2307/2026571Nordgreen, J., Garner, J. P., Janczak, A. M., Ranheim, B., Muir, W. M., &

Horsberg, T. E. (2009). Thermonociception in fish: effects of two different doses of morphine on thermal threshold and post-test behaviour in goldfish (Carassius auratus). Applied Animal Behaviour Science, 119(1–2), 101–107. https://doi.org/10.1016/j.applanim.2009.03.015

Norman, G. J., Karelina, K., Morris, J. S., Zhang, N., Cochran, M., & DeVries, A. C. (2010). Social interaction prevents the development of depressive-like behavior post nerve injury in mice: a potential role for oxytocin. Psychosomatic Medicine, 72(6), 519–526. https://doi.org/10.1097/PSY.0b013e3181de8678

Panksepp, J., Normansell, L., Cox, J. F., & Siviy, S. M. (1994). Effects of neonatal decortication on the social play of juvenile rats. Physiology & Behavior, 56(3), 429–443. https://doi.org/10.1016/0031-9384(94)90285-2

Panksepp, J., & Panksepp, J. B. (2013). Toward a cross-species understanding of empathy. Trends in Neurosciences, 36(8), 489–496. https://doi.org/10.1016/j.tins.2013.04.009

Pernick, M. S. (1985). A calculus of suffering: Pain, professionalism and anesthesia in Nineteenth Century America. New York: Columbia University Press.

Poole, J. (1998). An exploration of a commonality between ourselves and elephants. Etica & Animali, 9(98), 85–110.

Portavella, M. (2004). Avoidance response in Goldfish: Emotional and temporal involvement of medial and lateral telencephalic pallium. Journal of Neuroscience, 24(9), 2335–2342. https://doi.org/10.1523/JNEUROSCI.4930-03.2004

Preston, S. D., & de Waal, F. B. M. (2002a). Empathy: its ultimate and proximate bases. The Behavioral and Brain Sciences, 25(1), 1–20. https://doi.org/10.1017/S0140525X02000018

Preston, S. D., & de Waal, F. B. M. (2002b). The communication of emotions and the possibility of empathy in animals. In S. G. Post, L. G. Underwood, J. P. Schloss, & W. B. Hurlbut (Eds.), Altruistic Love: Science, Philosophy, and Religion in Dialogue (pp. 284–308). Oxford: Oxford University Press.

Reed, R. G., Randall, A. K., Post, J. H., & Butler, E. A. (2013). Partner influence and in-phase versus anti-phase physiological linkage in romantic couples. International Journal of Psychophysiology, 88(3), 309–316. https://doi.org/10.1016/j.ijpsycho.2012.08.009

Rowan, A. N. (1988). Animal anxiety and animal suffering, 20, 135–142.

37

Searle, J. (1994). Animal Minds. Midwest Studies In Philosophy, 19(1), 206–219.

Seth, A. K., Baars, B. J., & Edelman, D. B. (2005). Criteria for consciousness in humans and other mammals. Consciousness and Cognition, 14(1), 119–139. https://doi.org/10.1016/j.concog.2004.08.006

Shumaker, R., & Swartz, K. (2002). When traditional methodologies fail: Cognitive studies of great apes. In M. Bekoff, C. Allen, & G. M. Burghardt (Eds.), The Cognitive Animal (pp. 335–344). Cambridge: MIT Press.

Shutt, D. A., Fell, L. R., Connell, R., Bell, A. K., Wallace, C. A., & Smith, A. I. (1987). Stress-induced changes in plasma concentrations of immunoreactive ß-Endorphin and cortisol in response to routine surgical procedures in lambs. Australian Journal of Biological Sciences, 40(1), 97–104. https://doi.org/10.1071/BI9870097

Singer, T., & Lamm, C. (2009). The social neuroscience of empathy. Annals of the New York Academy of Sciences, 1156(1), 81–96. https://doi.org/10.1111/j.1749-6632.2009.04418.x

Smith, T. W., Cribbet, M. R., Nealey-Moore, J. B., Uchino, B. N., Williams, P. G., Mackenzie, J., & Thayer, J. F. (2011). Matters of the variable heart: respiratory sinus arrhythmia response to marital interaction and associations with marital quality. Journal of Personality and Social Psychology, 100(1), 103–19. https://doi.org/10.1037/a0021136

Sneddon, L. U. (2003). The evidence for pain in fish: the use of morphine as an analgesic. Applied Animal Behaviour Science, 83(2), 153–162. https://doi.org/10.1016/S0168-1591(03)00113-8

Sneddon, L. U. (2016). Anthropomorphic denial of fish pain. Animal Sentience, 10(Commentary on Key on fish Pain), 1–4.

Tye, M. (2000). Consciousness, Color, and Content. Cambridge: MIT Press.

Tye, M. (2016). Tense bees and shell-shocked crabs: Are animals conscious? New York: Oxford University Press.

Vanutelli, M. E., & Balconi, M. (2015a). Empathy and Prosocial Behaviours. Insights from Intra- and Inter-species Interactions. Rivista Internazionale Di Filosofia e Psicologia, 6(1), 88–109. https://doi.org/10.4453/rifp.2015.0007

Vanutelli, M. E., & Balconi, M. (2015b). Perceiving emotions in human–human and human–animal interactions: Hemodynamic prefrontal activity (fNIRS) and empathic concern. Neuroscience Letters, 605, 1–6. https://doi.org/10.1016/j.neulet.2015.07.020

38

Vanutelli, M. E., Gatti, L., Angioletti, L., & Balconi, M. (2017). Affective Synchrony and Autonomic Coupling during Cooperation : A Hyperscanning Study. BioMed Research International, 2017. https://doi.org/10.1155/2017/3104564

Vanutelli, M. E., Nandrino, J.-L., & Balconi, M. (2016). The boundaries of cooperation: Sharing and coupling from ethology to neuroscience. Neuropsychological Trends, 19(1). https://doi.org/10.7358/neur-2016-019-vanu

Varner, G. (1998). In nature’s interests? Interests, animal rights, and environmental ethics. New York: Oxford University Press.

Wall, P. D. (1979). On the relation of injury to pain. Pain, 6(3), 253–264. https://doi.org/10.1016/0304-3959(79)90047-2

Wall, P. D. (1992). Defining “pain in animals.” In C. E. Short & A. van Poznak (Eds.), Animal pain (pp. 63–79). New York: Churchill Livingstone.

Watanabe, S., & Ono, K. (1986). An experimental analysis of “empathic” response: effects of pain reactions of pigeon upon other pigeon’s operant behavior. Behavioural Processes, 13, 269–277. https://doi.org/10.1016/0376-6357(86)90089-6.

Weary, D. M., Niel, L., Flower, F. C., & Fraser, D. (2006). Identifying and preventing pain in animals. Applied Animal Behaviour Science, 100(1–2), 64–76. https://doi.org/10.1016/j.applanim.2006.04.013

Wechkin, S., Masserman, J. H., & Terris, W. (1964). Shock to a conspecific as an aversive stimulus. Psychonomic Science, 1, 47–48. https://doi.org/10.3758/BF03342783

Wöhr, M., & Schwarting, R. K. W. (2008). Ultrasonic calling during fear conditioning in the rat: no evidence for an audience effect. Animal Behaviour, 76(3), 749–760. https://doi.org/10.1016/j.anbehav.2008.04.017

Zahn-Waxler, C., Hollenbeck, B., & Radke-Yarrow, M. (1984). The origins of empathy and altruism. In M. W. Fox & L. D. Mickley (Eds.), Advances in animal welfare science (pp. 21–39). Washington: Humane Society of the United States.

Zentall, T. R. (2004). Action imitation in birds. Learning & Behavior: A Psychonomic Society Publication, 32(1), 15–23. https://doi.org/10.3758/BF03196003

Zimmerman, M. (1986). Physiological mechanisms of pain and its treatment. Klinische Anäesthesiol. Intensivtherapie, 32, 1–19.