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CAB Reviews 2018 13, No. 049

Pain sensitivity in

Paul Schroeder

Address: Department for Biomedical Services, Oxford University, The Old Observatory, South Parks Rd, Oxford, OX1 3RQ, UK.

Correspondence: Paul Schroeder. Email: [email protected]

Received: 9 August 2018 Accepted: 16 October 2018 doi: 10.1079/PAVSNNR201813049

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2018 (Online ISSN 1749-8848)

Abstract

The question of whether fish have the capacity to experience a state akin to was first empirically addressed by Jan Verheijen’s seminal study on in 1983. Subsequently, comprehensive evidence has been presented not only on the anatomical prerequisites for a pain system in several fish , but also for a behavioural component. Opinions against fish perceiving pain focus on the difference in neuroanatomy between higher and lower that do not possess a . Finally, the successful (behaviour sparing) use of can be interpreted as further evidence that fish are able to perceive pain and can be adversely affected by a painful event.

Keywords: Fish, Pain, , Analgesia

Review Methodology: The author searched the following databases, on or before 6th of August 2018: PubMed and Web of Science. Search terms included ‘fish & sentience’, ‘fish & pain’, ‘fish & pain & sensitivity’ and ‘fish & analgesia’. For the more general (introductory) section, the additional terms ‘pain & pathways’ and ‘ & pain’ were also used.

Introduction There are a range of pain categories according to location (deep, visceral, cutaneous) and duration (acute, Pain in has been defined as the unpleasant sensory chronic), with many possibilities for further gradation or emotional experience associated with actual or potential with respect to intensity and causation [4]. Pain is of tissue damage [1]. This -centred concept has primary concern when assessing if an animal study con- been expanded for that may not experience stitutes a regulated scientific procedure with the potential the same sensation to also incorporate the triggering to precipitate pain, , distress and lasting harm of protective motor actions, learned avoidance [2] and [5]. Animals cannot verbalize their pain so that in order a degree of awareness of damage or threat [3]. Bateson [4] to detect it the researcher has to rely on his or her expanded this concept further, identifying eight points interpretation of their behaviour [6] and [7]. indicative of the presence of pain in an animal: (1) poss- The lack of reliable assessment of has ession of functional receptors sensitive to noxious stimuli, been associated with variable pain relief in veterinary (2) possession of a structure analogous to the human medicine [7, 8]. , (3) possession of a nervous pathways Fish constitute more than half of all species of extant connecting nociceptive receptors to higher struc- vertebrates [9]. The question of whether fish possesses the tures, (4) possession of receptors for substances capacity for sentience remained largely unexplored until found in the central , (5) analgesics modify the 1980s, when Verheijen’s (1983) studies on showed the animal’s response to noxious stimuli and are chosen that these animals experienced similar sensations to pain by the animal when the experience is unavoidable, and fear when hooked and captured [10, 11]. Since then (6) animals respond to noxious stimuli by avoiding them there has been an increasing number of publications or minimizing damage to the body, (7) this avoidance focusing on endorsing the concept that fish have the behaviour is inelastic and (8) response to noxious stimuli capacity to suffer [12], including the ability to experience persists and the animal learns how to associate neutral pain beyond pure reflexes both in the context of sports events with noxious stimuli. [13] and experimentally generated pain [14].

http://www.cabi.org/cabreviews 2 CAB Reviews Receptors and Fibres nociceptive events could change the motivational state of , which resumed feeding later after injection with bee Pain has been described as a result of the stimulation of the venom or , compared with the group injected nociceptive system, a sensory system integral in an animal’s with saline. Braithwaite and Boulcoutt [25] argue that these control for preserving homoeostasis, beyond pure reflex three levels of analysis (anatomical, electrophysiological and responses [15]. is the detection of potentially behavioural) represent compelling evidence that injurious stimuli [16] that stimulate , receptors possess nociceptors and that their behaviour is affected by that preferentially detect damage. These primary sensory algesic stimuli. neurons are activated by stimuli signalling real or potential Opinions against fish perceiving pain focus on the differ- tissue damage [17] with their free nerve endings dispersed ence in neuroanatomy between humans and non- all over the body whilst their cell bodies are located in vertebrates such as fish that do not possess a neocortex the trigeminal (head) or dorsal root ganglia (spinal). There and have smaller with fewer neurons. Rose [26] are three main types of fibre type: free nerve suggests that the ‘conscious experience of fear and pain is a endings associated with myelinated A-β fibres mostly neurological impossibility’. Other authors argue that if detect innocuous stimuli in , muscle or joints though an improves the situation, this is proof that pain some contribute to pain; the more thinly myelinated A-δ was experienced [27], which supports the findings in the fibres (mostly linked to intense mechanical stimuli) and study [14] showing that significantly reduced thirdly the slower conducting unmyelinated C-fibres (linked pain-related behaviours. Apart from the behavioural to heat and chemical stimuli) are mainly associated with studies mentioned above, pain perception in fish has been detection of noxious stimuli [18]. Five percent of all endorsed through the identification of opioid receptors in C-nociceptors fire to mechanical stimuli only [19] and the animals’ nervous tissue [27, 28]. some can also register itch and innocuous temperatures [17]. Nociceptors have been identified in mammals, , reptiles and teleosts but not in the older clades Reponses to of elasmobranchs or . In lampreys receptors sen- sitive to noxious stimuli were identified, though respon- Pain perception in fish is likely to differ from human experi- siveness was only intermittent [20]. Despite the lack ence and may not be consistent with our understanding of conclusive evidence for nociceptors in chordate taxa of mammalian physiology [29, 30]. Rather than ruling predating teleosts, unmyelinated structures resembling out pain on the basis of mere anatomical differences, C-fibres were found in hagfish and myelinated A-δ fibres judgements should be made based on evidence. For were found in elasmobranchs. example, as a starting point, the understanding of pain in While both A-δ and C-fibres are found in higher a particular group of animals can be based upon behavioural vertebrates and fish; the latter constitute 60% or physiological changes linked to painful events in other of fibres in skin [21] and also the majority of fibre species, such as post-surgically increased respiratory rates type found in other mammals, birds and amphibians in and dogs and a higher opercular beat rate for fish [19, 22] but only 4% of the fibre type found in teleosts [16]. subjected to trauma [29]. Several studies attempt to link behavioural and physio- logical responses: Fin-clipped ( Evidence for Pain in Fish niloticus) showed that there was an increase in time spent in the illuminated section of the tank accompanied by Of Bateson’s criteria for defining pain in animals (1991) an increase in swimming activity. A further observation suggesting that a number of factors exceeding nociception interpreted as pain response was the emptying of mucus would need to be in place to constitute an emotional state cells in the gills, usually associated with stressful events [31] whereby suffering or discomfort is experienced, several and recorded 1 h after the fin clip. The same study also have been identified in fish: the reaction to a noxious found a significant increase in plasma yet there was stimulus by avoidance or damage minimization was shown no information on time elapsed post-surgery. The study for pike as early as 1970 [23]. The inelastic avoidance was not able to discriminate between the stress imposed response and learned pain association were shown for by the clip and that by handling stress. and trout [24]. A study focusing on thermonociception in goldfish Exploring both the anatomical and behavioural com- (Carassius auratus) reported an escape response modulated ponents of a pain system in fish, Sneddon [14] found by administration of morphine, when an attached thermal three nociceptor types (polymodal, mechanochemical and device became too hot [32]. Investigations of post- mechanothermal) on the head of . The same nociceptive behaviours in rainbow trout ( study also confirmed the presence of A-δ and C-fibres in mykiss) [14]; (Cyprinus carpio) and the trigeminal ganglion of the same species, and recorded (Danio rerio) [33, 34] established that the type and neural activity from cells in the ganglion after stimulation of magnitude of behavioural patterns after painful events, the nociceptors. The work concluded by showing that in this case injection of acetic acid, was species specific.

http://www.cabi.org/cabreviews Paul Schroeder 3 The studies also showed that an increased ventilation rate test-challenged and control fish suggesting deleterious side was indicative of nociceptive stimuli in zebrafish and trout effects [38]. but not in carp. In the same study, zebrafish displayed More recently, several immersion drugs were trialled a reduced swim rate, measured as direct movement longer with varying effect on zebrafish. administered than one body length, whereas rainbow trout showed at 5 mg/l has been shown to modulate post-nociceptive an increase. No change in activity was observed in behaviour after a tail fin clip [43] and noxious temperature common carp [14, 34]. Injection of acetic acid into the lip stimuli [44]. For larval zebrafish morphine (48 mg/l) elicited ‘lip rubbing’ in rainbow trout, an atypical behaviour immersion proved efficacious [44], possibly due to better thought to be analogous to humans rubbing painful areas, gill permeability for this type of molecule in . although this causality has not been accepted by everyone [35], but is not seen in control fish. This particular behavioural response has also been recorded in goldfish Diverging Views on Pain Sensitivity in Fish experiencing a painful event [36]. A potentially analogous response has been observed in zebrafish, where after acid The alternative view, that due to their brain anatomy injections near the tailfin animals have reacted with rapid (lack of a human neocortex) fish lack the true capacity to fin movements described as ‘tailfin fanning’ [34]. have and feel pain [26, 35, 45, 46], is based Behavioural changes were also reported when goldfish upon mammalian neuroscience studies [46, 47] though were exposed to high-intensity electric shocks. They these have prompted other comparative anatomists [48] responded by freezing, then fast escape (‘panic swimming’) to propose the opposite (i.e. that all vertebrates are or a calmer escape response. The animals rarely responded conscious). The universal validity of the classical view in to lower currents with fast escape, indicative that the comparative neuroanatomy that structure dictates function animal’s response magnitude was tied to the intensity of the has been comprehensively challenged [49] and several stimulus [24]. These examples show that fish respond to studies exist that confirm the opposite [50, 51]. For a range of painful stimuli while the resulting behavioural example, with the same logic neither reptiles nor birds changes are subject to great variation between species, would have the capacity to experience pain yet conclusive even closely related ones such as zebrafish and carp. evidence exists that the avian has developed neocortex-like cognitive functions reflecting the functional rather than structural homologies between avian and Use of Analgesia mammalian brains [49, 52, 53]. Thus, it is intuitive to suggest that fish that have evolved in an aquatic environ- The fact that there is an increase in the time spent between ment have also developed a different brain structure a nociceptive stimulus and the return to feeding compared to perform these functions. Those opposed to the view with a non-nociceptive control stimulus has been used as that fish can perceive pain also present the argument that proof that the animal’s behaviour is adversely affected by a avoidance and self-administration of analgesics in potentially painful event [37]. Compounds which pain response to painful stimuli can occur unconsciously, and indicators favourably have been described as ‘behaviour- that they consequently represent no step up from simple sparing’ [38] as they allow more natural behaviour. nociception. Yet the actual evidence provided here appears For smaller ornamental or research species such as cave to consist of a single human autopsy report [45]. Along fish (Astyanax mexicanus), zebrafish (D. rerio) or medaka with others the same author later asserts that the burden (Oryzias latipes), their relatively small size (usually less than of proof is with those supporting the concept that fish 1 g), means that intramuscular or subcutaneous injections can suffer or feel pain [53]. The proponents of this view become difficult to administer without undue trauma as target the perceived feeling-based approach to fish welfare opposed to larger fish where this is the most effective route as anthropomorphic speculation [26, 35, 45, 54] but ignore for perioperative analgesia [39]. Intraperitoneal injections, that the general definitions supporting this approach particularly in smaller fish, entail the risk of site specific [11, 55, 56] have become well-established tenets of adverse effects [40]. Absorption through gills varies modern science. The interpretation of between drugs since lipophilic compounds diffuse across studies which have supported the concept of sentience gill membranes while ions do not [41]. Choice of agents is and fish’ capacity to experience pain has also been chal- also limited by water solubility. lenged on perceived weaknesses in experimental design. Ketoprofen (Ketofen®) has been used in Koi carp For example, the increased opercular rate observed after surgery and while it has not shown any behaviour-sparing injection of acetic acid into the lips of trout [57] was attrib- effects when administered postoperatively it had anti- uted by Rose to ‘acid leaching into the gills’ [35]. However, inflammatory effects at 2 mg/kg i.m., reducing the indicators other studies exploring algesiogenic stimuli at locations of muscle damage [42]. Carprofen was investigated in much further away from the gills also recorded increased rainbow trout challenged with painful stimuli. Fish resumed opercular rate [43] or changes in gill histology [31]. feeding more quickly than fish with no analgesia but a dose More recently, in a joint review article [58], those of 5 mg/kg resulted in depressed activity in both acetic acid opposed to the concept of pain and sentience in fish have

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