Trigeminal Somatosensory Innervation of the Head of a Teleost Fish with Particular Reference to Nociception

Trigeminal somatosensory receptors have not been characterised in teleost fish and studies in elasmobranchs have failed to identify nociceptors. The present study examined the trigeminal nerve of a teleost fish, the rainbow trout (Oncorhynchus mykiss) to determine what types of somatosensory receptors were present on the head of the trout specifically searching for nociceptors. Single unit recordings were made from receptive fields on the head of the fish innervated by the trigeminal nerve. Each receptive field was tested for sensitivity to mechanical, thermal and chemical stimulation. Five different receptor types were found: fast adapting receptors responding to mechanical stimulation; slowly adapting receptors responding to mechanical stimuli; polymodal nociceptors responding to mechanical, noxious thermal and chemical stimulation; mechanothermal nociceptors responding to mechanical stimulation and noxious heat; and mechanochemical receptors responsive to mechanical and chemical stimulation. Mechanical thresholds, receptive field diameter, conduction velocities and thermal thresholds of the receptors were determined and there was no significant difference between the receptor types in terms of these properties. Three shapes of action potential (AP) were recorded from these receptors: type 1 with no inflexion; type 2 with an inflexion on depolarisation; and type 3 with an inflexion on repolarisation. Conduction velocity, amplitude and duration of the APs, after hypolarisation amplitude and duration, as well as the maximum rate of depolarisation were measured for each action potential type. No major differences were found when making comparisons within receptor type and between receptor types. The fish nociceptors had similar physiological properties to nociceptors found in higher vertebrates

Evolution of Nociception in Vertebrates: Comparative Analysis of Lower Vertebrates

Nociception is an important sensory system of major fundamental and clinical relevance. The nociceptive system of higher vertebrates is well studied with a wealth of information about nociceptor properties, involvement of the central nervous system and the in vivo responses to a noxious experience are already characterised. However, relatively little is known about nociception in lower vertebrates and this review brings together a variety of studies to understand how this information can inform the evolution of nociception in vertebrates. It has been demonstrated that teleost fish possess nociceptors innervated by the trigeminal nerve and that these are physiologically similar to those found in higher vertebrates. Opioid receptors and endogenous opioids are found in the brain and spinal cord of the fishes and morphine blocks avoidance learning using electric shock as well as reducing nociceptive behavioural and physiological responses to noxious stimulation. Comparative analysis of the fishes and higher vertebrates show that fish possess less C fibres than higher vertebrates. The electrophysiological properties of fish nociceptors are almost identical to those found in higher vertebrates suggesting the evolution of these properties occurred before the emergence of the fish groups

Pain Perception in Fish: Evidence and Implications for the Use of Fish

Pain assessment in fish is particularly challenging due to their evolutionary distance from humans, their lack of audible vocalization, and apparently expressionless demeanour. However, there are criteria that can be used to gauge whether pain perception occurs using carefully executed scientific approaches. Here, the standards for pain in fish are discussed and can be considered in three ways: neural detection and processing of pain; adverse responses to pain; and consciously experiencing pain. Many procedures that we subject fish to cause tissue damage and may give rise to the sensation of pain. Fish are popular as pets, in animal exhibits, and as experimental models, but are also cultured or caught for food. There is little legislation for the protection of fish welfare. Many countries are now exploring the welfare cost to fish, and current practices may need to be reviewed with respect to the current evidence for fish perceiving pain

Pain Perception in Fish: Indicators and Endpoints

Recent evidence has shown that fish display aversive behavioral and physiological reactions and a suspension of normal behavior in response to noxious stimuli that cause pain in other animals and humans. In addition to these behavioral responses, scientists have identified a peripheral nociceptive system and recorded specific changes in the brain activity of fish during noxious stimulation. As a result of these observations teleost fish are now considered capable of nociception and, in some opinions, pain perception. From both an experimental and an ethical perspective, it is important that scientists be able to assess possible pain and minimize discomfort that may result from invasive or other noxious procedures. If scientists accept that the definition of pain in animals cannot include direct measurement of subjective experience (the standard for humans), then fish fulfill the criteria for animal pain. In this review, recent evidence for pain is discussed in terms of the physiological properties of nociceptors, central responses to noxious stimulation, and changes in behavior and physiology that are indicative of nociception and are responsive to analgesia. To enable the assessment of potential pain, there are descriptions of newly identified robust indicators and species-specific responses that are easily measurable. The article concludes with a discussion of humane endpoints and of the need for alleviation of pain through the use of analgesia and anesthesia

Clinical Anesthesia and Analgesia in Fish

Fish have become a popular experimental model and companion animal, and are also farmed and caught for food. Thus, surgical and invasive procedures in this animal group are common, and this review will focus on the anesthesia and analgesia of fish. A variety of anesthetic agents are commonly applied to fish via immersion. Correct dosing can result in effective anesthesia for acute procedures as well as loss of consciousness for surgical interventions. Dose and anesthetic agent vary between species of fish and are further confounded by a variety of physiological parameters (e.g., body weight, physiological stress) as well as environmental conditions (e.g., water temperature). Combination anesthesia, where 2 anesthetic agents are used, has been effective for fish but is not routinely used because of a lack of experimental validation. Analgesia is a relatively underexplored issue in regards to fish medicine. However, recent studies have investigated opioid agents, nonsteroidal anti-inflammatory drugs, and local anesthetics to determine their efficacy in minimizing pain and discomfort. The opioid morphine and the local anesthetic lidocaine do have significant effectiveness in reducing pain-related responses in rainbow trout (Oncorhynchus mykiss). Studies aimed at developing reliable analgesic protocols should explore a wide range of analgesic drug classes in several fish species

Fish Behaviour and Welfare

Fish are farmed intensively in aquaculture which is an economic necessity to provide large quantities for the food industry yet many species’ normal behaviours may be impaired by the nature of intensive aquaculture. Recommendations have suggested that for optimum welfare, animals should be able to express their natural suite of behaviours. Confining large migratory species such as salmonids to relatively small tanks or cages means they are unable to perform the extensive migrations performed by their wild counterparts so are these fish frustrated? When considering why salmonids migrate, their motivation is to find food yet if they are well fed by the farmer does this dampen the desire to migrate? The conflict of behavioural needs and the major welfare issues in aquaculture highlighted by recent scientific studies are discussed by Ashley. Species specific requirements are an important issue since fishes are one of the most diverse vertebrate taxa on the globe. Salmonids require the ability to swim constantly whereas flatfishes require ample space to rest on the substrate. When space is limited for flatfish, such as the commercially important halibut, they perform stereotypical surface swimming which has not been observed outside of the fish farm. Kristiansen and Fernö investigate individual variation in response to floating or sinking food pellets and find that stress coping style results in some individuals showing poor growth when fed floating food but their well-being improves when given food that sinks. These small changes in aquaculture procedures can make a real difference to fish growth and hence improve welfare and economic return

Anatomical and Electrophysiological Analysis of the Trigeminal Nerve in a Teleost Fish, Oncorhynchus mykiss

The trigeminal nerve in the rainbow trout, Oncorhynchus mykiss, was examined for the presence of A-delta and C fibres. Sections of the three branches of the trigeminal nerve were found to comprise a range of fibre types including Adelta and C fibres. The size range of the cell bodies of the trigeminal ganglion reflected the fibre range since they correlated with the size range of axons in the nerve branches. Electrophysiological recordings of evoked activity from the ganglion confirmed the presence of these fibre types and the proportion of these mirrored the proportion of fibre types in the anatomical analyses. A-beta fibres were most common followed by A-delta fibres, then A-alpha fibres with C fibres being the fewest fibre type found. In higher vertebrates, A-delta and C fibres in the trigeminal nerve convey both somatosensory and nociceptive information to the brain. The evolutionary significance of these results is discussed as well as the potential for nociceptive capability in a lower vertebrate

Pain in Aquatic Animals

Recent developments in the study of pain in animals have demonstrated the potential for pain perception in a variety of wholly aquatic species such as molluscs, crustaceans and fish. This allows us to gain insight into how the ecological pressures and differential life history of living in a watery medium can yield novel data that inform the comparative physiology and evolution of pain. Nociception is the simple detection of potentially painful stimuli usually accompanied by a reflex withdrawal response, and nociceptors have been found in aquatic invertebrates such as the sea slug Aplysia. It would seem adaptive to have a warning system that allows animals to avoid life-threatening injury, yet debate does still continue over the capacity for non-mammalian species to experience the discomfort or suffering that is a key component of pain rather than a nociceptive reflex. Contemporary studies over the last 10 years have demonstrated that bony fish possess nociceptors that are similar to those in mammals; that they demonstrate pain-related changes in physiology and behaviour that are reduced by painkillers; that they exhibit higher brain activity when painfully stimulated; and that pain is more important than showing fear or anti-predator behaviour in bony fish. The neurophysiological basis of nociception or pain in fish is demonstrably similar to that in mammals. Pain perception in invertebrates is more controversial as they lack the vertebrate brain, yet recent research evidence confirms that there are behavioural changes in response to potentially painful events. This review will assess the field of pain perception in aquatic species, focusing on fish and selected invertebrate groups to interpret how research findings can inform our understanding of the physiology and evolution of pain. Further, if we accept these animals may be capable of experiencing the negative experience of pain, then the wider implications of human use of these animals should be considered

The Evidence for Pain in Fish: The Use of Morphine as an Analgesic

This paper discusses the evidence for pain perception in fish and presents new data on morphine analgesia in fish. Recent anatomical and electrophysiological studies have demonstrated that fish are capable of nociception, the simple detection of a noxious, potentially painful stimulus and the reflex response to this. To prove pain perception, it must be demonstrated that an animal’s behaviour is adversely affected by a potentially painful event and this must not be a reflex response. The present study examined the acute effects of administering a noxious chemical to the lips of rainbow trout (Oncorhynchus mykiss) to assess what changes occurred in behaviour and physiology. There was no difference in swimming activity or use of cover when comparing the noxiously stimulated individuals with the controls. The noxiously treated individuals performed anomalous behaviours where they rocked on either pectoral fin from side to side and they also rubbed their lips into the gravel and against the sides of the tank. Opercular beat rate (gill or ventilation rate) increased almost double fold after the noxious treatment whereas the controls only showed a 30% increase. Administering morphine significantly reduced the pain-related behaviours and opercular beat rate and thus morphine appears to act as an analgesic in the rainbow trout. It is concluded that these pain-related behaviours are not simple reflexes and therefore there is the potential for pain perception in fish

Do painful sensations and fear exist in fish?

The detection of pain and fear in fi sh has been subject to much debate and, since fi sh are a popular experimental model and commercially important in both angling and aquaculture, many procedures that fi sh are subjected to cause injury, fear and stress. These injuries would give rise to the sensation of pain in humans but whether fi sh have the capacity for pain is relatively under explored. Recent evidence has shown that fi sh have the same neural apparatus to detect pain that mammals and humans do, that their brain is active during a potentially painful experience, that fi sh show negative changes in behaviour and physiology and that this is reduced by administering a pain killer. Experiments demonstrating the signifi cance of pain to fi sh have been conducted and have shown that fi sh do not show appropriate fear and anti- predator responses during a painful stimulation. This suggests that they are dominated by the pain state confi rming its importance to the fi sh. However, social context affects the aggressive behaviour of fi sh when noxiously stimulated. In a familiar group, dominant trout perform much less chasing of conspecifi cs yet this suspension in aggression is not seen when placed in an unfamiliar group of fi sh. Therefore, responses to pain are more complex and not simple refl exes. Together, these results demonstrate that pain is an important stimulus for a trout and we should seek to minimise and alleviate pain where possible. Studies have demonstrated that fi sh are capable of exhibiting signs of fear including avoidance behaviour and they may also anticipate fearful events. Recent evidence shall be discussed with future directions suggested