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Journal ArticleDOI

Novel Object Test: Examining Nociception and Fear in the Rainbow Trout

01 Oct 2003-The Journal of Pain (Churchill Livingstone)-Vol. 4, Iss: 8, pp 431-440
TL;DR: Results suggest that nociception captures the animal's attention with only a relatively small amount of attention directed at responding to the fear of the novel object.
About: This article is published in The Journal of Pain.The article was published on 2003-10-01 and is currently open access. It has received 217 citations till now. The article focuses on the topics: Noxious stimulus.

Summary (3 min read)

Introduction

  • This study aimed to assess fear responses to a novel object while experiencing a noxious event to determine whether nociception or fear will dominate attention in a fish in novel object testing paradigm.
  • Control animals displayed a classic fear response to the novel objects and spent most of their time moving away from this stimulus, as well as showing an increase in respiration rate when the novel object was presented.
  • In particular, research on learning42 and memory tasks25,65 such as concentration33 or attentiveness15 have demonstrated that in humans pain predominates attention and has a negative impact on performance of such tasks.
  • The behavioral responses to acute noxious stimulation have been established in this fish, as well as the neurophysiology of the trigeminal nociceptors, which have similar properties to mammalian nociceptors.
  • The relationship between pain and fear is probably dynamic and the direction of the influence might vary with the situation, and so this study also examines the question of whether a noxious stimulus attenuates the fear response to a novel stimulus.

Materials and Methods

  • Each tank had a flow through supply of filtered fresh water kept at approximately 14°C.
  • The tanks also had transparent tape fixed along the bottom and sides of the tank with a centimeter scale drawn on by a waterproof marker pen.
  • Once a fish had successfully learned this task and performed it for 8 consecutive trials, it was assumed that its behavior was normal or stress free because it could acquire a learning task and it was ingesting food.
  • Experimental protocols were approved by the Roslin Institute’s Ethical Review Board.

Test Group 1: Response to a Novel Object

  • Observations were made on each fish twice for 30 minutes (AM and PM) to record normal opercular beat rate (OBR) (gill movements).
  • 71 Acetic acid was chosen because the protons of the acid stimulate nociceptive nerves in mammals.
  • After this 5-minute observation period, a novel object was slowly lowered into the tank so not to startle the fish and was placed approximately 10 cm from the head of the fish.
  • Once the object had been present for 15 minutes, it was carefully removed.
  • Novel object presentation was repeated an additional 4 times at hourly intervals, and at each presentation a differently shaped and colored novel object was used.

Test Group 2: Response to a Familiar Object

  • A different set of fish (n = 10) in this test group were trained on the conditioning task as described above except that after they had successfully performed the task 4 times, they had 1 of the objects carefully placed into their tank after the AM training trial and removed after the PM training trial.
  • This was done for 4 days before testing so that the fish could become familiar with the object and were exposed to it for approximately 8 hours per day.
  • The AM observation was made without the object being present, whereas the PM observation did have the object present.
  • Therefore, the distance that the fish was from the familiar object could be recorded and compared with the results from day 2.

Test Group 3: Response to a Novel Object After Morphine Administration

  • This analgesic dose was previously used by Ehrensing et al19 to block the learning of aversive conditioning by using electric shock in goldfish, and this was reversed by using naloxone.
  • Diffusion time for morphine after intramuscular injection is not known in fish, but previous work has shown that it took approximately 10 minutes for intramuscularly injected pancuronium to be effective (unpublished observation).
  • Therefore, the 30-minute recovery period after morphine injection is likely to be sufficient time for the analgesic to have diffused into the blood and body tissues.

Statistical Analyses

  • The data were not normally distributed, so nonparametric tests were used throughout.
  • These distances were chosen because nearer than 5 cm was closer in proximity to where the object was originally placed and greater than 10 cm was a direct movement away from the object, whereas between 5 and 10 cm might indicate no particular movement toward or away from the object.
  • The proportion of time spent at less than 5 cm and greater than 10 cm was compared between the Acid and Control groups by using Kruskal-Wallis tests, as was the latency to approach the object within each test group and between test groups.
  • Respiration rate was compared for the mean value of day 1 with the mean for day 2 both before and after novel object presentation by using a Kruskal-Wallis test.
  • The tests were performed within test group to compare Control and Acid groups but also between test groups to understand the differences between neophobia, familiarity, and morphine analgesia.

Time Spent Moving to and Moving Away From the Object

  • This pattern was similar for the first presentation time, but there were no significant differences between the Acid and Control groups at presentation times 2, 4, and 5 (Table 1).
  • At presentation time 3, the Control group spent less time within 5 cm than the Acid group, but the reverse was true for time spent at more than 10 cm (Table 1).

Discussion

  • The control animals in Test Group 1 displayed a classic neophobia to a novel object because they took a relatively long time to approach the object, they spent very little time in close proximity, and the majority of their time was spent moving away from the novel object.
  • They did show reduced nociception-related behaviors, rocking and rubbing, compared with the frequency of these behaviors before presenting the object.
  • The analgesic effects of morphine are well-known in animals and humans;17,39,53 however, virtually no work has been done on analgesia in fish.
  • The present study has shown that the trout’s response to noxious stimulation is complicated in nature.

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Journal ArticleDOI
TL;DR: The scientific data that allows us to interpret the effects of disease, handling, transport, food deprivation, and slaughter technique on fish welfare are reviewed and caution should be taken when interpreting "abnormal" fish behaviour.

847 citations


Cites background from "Novel Object Test: Examining Nocice..."

  • ...…the potential to experience suffering in the form of pain and fear (for review see Braithwaite and Huntingford, 2004; Chandroo et al., 2004a,b; Ashley and Sneddon, in press; empirical studies include Portavella et al., 2003, 2004a,b; Sneddon, 2003; Sneddon et al., 2003a,b; Dunlop and Laming, 2005)....

    [...]

Journal ArticleDOI
TL;DR: This paper focuses on welfare as the absence of suffering in fish, arguing that complex animals with sophisticated behaviour, such as fish, probably have the capacity for suffer ing, though this may be different in degree and kind from the human experience of this state.
Abstract: Human beings may affect the welfare of fish through fisheries, aquaculture and a number of other activities. There is no agreement on just how to we igh the concern for welfare of fish against the hum an interests involved, but ethical frameworks exist th at suggest how this might be approached. Different definitions of animal welfare focus on an animal's condition, on its subjective experience o f that condition and/or on whether it can lead a natu ral life. These provide different, legitimate, pers pectives, but the approach taken in this paper is to focus on welfare as the absence of suffering. An unresolved and controversial issue in discussion s about animal welfare is whether non-human animals exposed to adverse experiences such as physical injury or confinement experience what humans would call suffering. The neocortex, which in huma ns is an important part of the neural mechanism tha t generates the subjective experience of suffering, i s lacking in fish and non-mammalian animals, and it has been argued that its absence in fish indicates that fish cannot suffer. However, a strong alternative view is that complex animals with sophisticated behaviour, such as fish, probably have the capacity for suffer ing, though this may be different in degree and kind fro m the human experience of this state. Recent empirical studies support this view and show that painful stimuli are, at least, strongly avers ive to fish. Consequently, injury or experience of othe r harmful conditions is a cause for concern in term s of welfare of individual fish. There is also growing e vidence that fish can experience fear-like states a nd that they avoid situations in which they have experience d adverse conditions.

690 citations


Cites background or result from "Novel Object Test: Examining Nocice..."

  • ...The fact that exposure to noxious stimuli interferes with the normal neophobic responses suggests that fish give a high priority to such stimul (Sneddon et al., 2003b)....

    [...]

  • ...…Oncorhynchus mykiss), however, anatomical and electrophysiological examination of the trigeminal erve (which is known to convey pain information from the head and mouth in terrestrial vertebrates) has identified two types of nociceptor, A-delta and C fibres (Sneddon, 2002; Sneddon et al., 2003a)....

    [...]

  • ...Similar studies have also sh wn that the adverse behaviour of fish under noxious Journal of Fish Biology by Wiley-Blackwell For more articles on animal ethics, see www.animalethics.net stimulation can be mitigated if an analgesic (morphine) is administered (Sneddon et al., 2003b)....

    [...]

  • ...In support of this point, recent behavioural experiments have demonstrated effects of noxious stimulations around the mouth of rainbow trout (Sneddon et al., 2003a)....

    [...]

  • ...…(Furevik et al., 1993) and to tissue damage (for example, carp that are hooked in the mouth show rapid darting, spitting a d shaking of the head (Verheijen & Buwalda, 1988) and rainbow trout injected with acetic acid in their lips rub their snouts against the substratum (Sneddon et al., 2003)....

    [...]

Journal ArticleDOI
TL;DR: Criteria that demonstrate, beyond a reasonable doubt, whether animals of a given species experience pain are defined that are vital to inform whether to alleviate pain or to drive the refinement of procedures to reduce invasiveness.

307 citations


Cites background from "Novel Object Test: Examining Nocice..."

  • ...For example, trout will ignore novel objects in fear tests rather than show neophobia when in apparent pain; however, this is reversed when morphine is administered (Sneddon et al., 2003b)....

    [...]

Journal ArticleDOI
TL;DR: This review summarises the main findings on how behavioural changes have been used to assess welfare in farmed fish, using both functional and feeling-based approaches and underlines the need to develop on-farm, operational behavioural welfare indicators that can be easily used to assessed not only the individual welfare but also the welfare of the whole group.
Abstract: Behaviour represents a reaction to the environment as fish perceive it and is therefore a key element of fish welfare. This review summarises the main findings on how behavioural changes have been used to assess welfare in farmed fish, using both functional and feeling-based approaches. Changes in foraging behaviour, ventilatory activity, aggression, individual and group swimming behaviour, stereotypic and abnormal behaviour have been linked with acute and chronic stressors in aquaculture and can therefore be regarded as likely indicators of poor welfare. On the contrary, measurements of exploratory behaviour, feed anticipatory activity and reward-related operant behaviour are beginning to be considered as indicators of positive emotions and welfare in fish. Despite the lack of scientific agreement about the existence of sentience in fish, the possibility that they are capable of both positive and negative emotions may contribute to the development of new strategies (e.g. environmental enrichment) to promote good welfare. Numerous studies that use behavioural indicators of welfare show that behavioural changes can be interpreted as either good or poor welfare depending on the fish species. It is therefore essential to understand the species-specific biology before drawing any conclusions in relation to welfare. In addition, different individuals within the same species may exhibit divergent coping strategies towards stressors, and what is tolerated by some individuals may be detrimental to others. Therefore, the assessment of welfare in a few individuals may not represent the average welfare of a group and vice versa. This underlines the need to develop on-farm, operational behavioural welfare indicators that can be easily used to assess not only the individual welfare but also the welfare of the whole group (e.g. spatial distribution). With the ongoing development of video technology and image processing, the on-farm surveillance of behaviour may in the near future represent a low-cost, noninvasive tool to assess the welfare of farmed fish.

300 citations


Cites background from "Novel Object Test: Examining Nocice..."

  • ...Other examples, although not in an aquaculture context, come from exposing rainbow trout to noxious stimuli, which has been shown to affect an individual’s exploratory behaviour (Sneddon et al. 2003)....

    [...]

Journal ArticleDOI
TL;DR: B Bold fishes given negative experiences reduced their boldness which may be an adaptive response; however, shy fishes may base their strategic decisions upon self-assessment of their relative competitive ability and increase theirboldness in situations where getting to resources more quickly ensures they outcompete better competitors.
Abstract: Theoreticians predict that animal ‘personality’ traits may be maladaptive if fixed throughout different contexts, so the present study aimed to test whether these traits are fixed or plastic. Rainbow trout (Onchorhyncus mykiss) were given emboldening or negative experiences in the forms of watching bold or shy individuals responding to novelty or winning or losing fights to examine whether prior experience affected boldness. Bold individuals that lost fights or watched shy demonstrators became more shy by increasing their latency to approach a novel object, whereas shy observers that watched bold demonstrators remained cautious and did not modify their responses to novelty. Shy winners became bolder and decreased their latency to approach a novel object, but shy losers also displayed this shift. In comparison, control groups showed no change in behaviour. Bold fishes given negative experiences reduced their boldness which may be an adaptive response; however, shy fishes may base their strategic decisions upon self-assessment of their relative competitive ability and increase their boldness in situations where getting to resources more quickly ensures they outcompete better competitors.

292 citations


Cites background or methods from "Novel Object Test: Examining Nocice..."

  • ...…= 2.5; KMO = 0.937; p < 0.001; d.f. = 10) and as this is a standard paradigm used in humans, mammals and fishes (Wilson et al. 1993, 1994; Wilson 1998; Sneddon et al. 2003; Schjolden et al. 2005), the data on 5 cm latency is used as the primary indicator of boldness in the following results....

    [...]

  • ...Novel objects consisted of Lego bricks constructed to produce objects of various colours, sizes and dimensions to a maximum of 10 x 7 x 4 cm, as used by Sneddon et al. (2003)....

    [...]

  • ...The novel object, as described previously, was different for each presentation to prevent habituation, since it has been shown that using novel objects of different colours and shapes continues to elicit a fear response in rainbow trout when presented consecutively (Sneddon et al. 2003)....

    [...]

References
More filters
Journal ArticleDOI
TL;DR: The need to make direct measurement of poor welfare as well as to use sophisticated studies of animal preferences is emphasized and the uses of measures of responsiveness, stereotypies, and animal preferences in welfare assessment are discussed.
Abstract: The term “welfare” refers to the state of an individual in relation to its environment, and this can be measured. Both failure to cope with the environment and difficulty in coping are indicators of poor welfare. Suffering and poor welfare often occur together, but welfare can be poor without suffering and welfare should not be defined solely in terms of subjective experiences. The situations that result in poor welfare are reviewed in this study with special reference to those in which an hdividual lacks control over interactions with its environment. The indicators of poor welfare include the following: reduced life expectancy, impaired growth, impaired reproduction, body damage, disease, immunosup pression, adrenal activity, behavior anomalies, and self-narcotization. The uses of measures of responsiveness, stereotypies, and animal preferences in welfare assessment are discussed. The need to make direct measurement of poor welfare as well as to use sophisticated studies of animal preferences is emphasized.

837 citations

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09 May 1980-Science
TL;DR: Depending only on its temporal characteristics, foot-shock stress appears to activate opioid or nonopioid analgesia mechanisms, certain forms of stress may act as natural inputs to an endogenous opiate analgesia system.
Abstract: Inescapable foot shock in rats caused profound analgesia that was antagonized by naloxone or dexamethasone when shock was delivered intermittently for 30 minutes, but not when it was delivered continuously for 3 minutes. Thus, depending only on its temporal characteristics, foot-shock stress appears to activate opioid or nonopioid analgesia mechanisms. Certain forms of stress may act as natural inputs to an endogenous opiate analgesia system.

713 citations

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01 Feb 2002-Pain
TL;DR: This paper compares the modulatory influences of two principal cognitive variables, attention and emotion, on pain perception and addresses possible neural mechanisms underlying each of these influences.
Abstract: There have been anecdotal accounts for centuries of people apparently experiencing little or no pain in situations that most of us would find excruciating. Yet, western medicine has given little credence to a patient’s ability to modify pain. Instead, we focus on the pharmacological control of pain. For this reason, the vast majority of research on pain control has concentrated on peripheral and spinal cord mechanisms of opioid and anti-inflammatory analgesic therapy. Nevertheless, researchers are beginning to recognize that a variety of pain modulatory mechanisms exist in the nervous system, and these modulatory systems can be accessed either pharmacologically or through contextual and/or cognitive manipulation (Fields, 2000). Variables such as attentional state, emotional context, hypnotic suggestions, attitudes, expectations or anesthesia-induced changes in consciousness now have been shown to alter both pain perception and forebrain pain transmission in humans. These techniques, at times, preferentially alter sensory and/or affective aspects of pain perception, and the associated modulation of pain-evoked neural activity occurs in limbic and/or sensory brain regions, suggesting multiple endogenous pain-modulatory systems. This paper compares the modulatory influences of two principal cognitive variables, attention and emotion, on pain perception and addresses possible neural mechanisms underlying each of these influences.

611 citations

Journal ArticleDOI
01 Mar 2000-Pain
TL;DR: It is argued that VR is a uniquely attention‐capturing medium capable of maximizing the amount of attention drawn away from the ‘real world’, allowing patients to tolerate painful procedures, and merits more attention as a potentially viable form of treatment for acute pain.
Abstract: For daily burn wound care procedures, opioid analgesics alone are often inadequate. Since most burn patients experience severe to excruciating pain during wound care, analgesics that can be used in addition to opioids are needed. This case report provides the first evidence that entering an immersive virtual environment can serve as a powerful adjunctive, nonpharmacologic analgesic. Two patients received virtual reality (VR) to distract them from high levels of pain during wound care. The first was a 16-year-old male with a deep flash burn on his right leg requiring surgery and staple placement. On two occasions, the patient spent some of his wound care in VR, and some playing a video game. On a 100 mm scale, he provided sensory and affective pain ratings, anxiety and subjective estimates of time spent thinking about his pain during the procedure. For the first session of wound care, these scores decreased 80 mm, 80 mm, 58 mm, and 93 mm, respectively, during VR treatment compared with the video game control condition. For the second session involving staple removal, scores also decreased. The second patient was a 17-year-old male with 33.5% total body surface area deep flash burns on his face, neck, back, arms, hands and legs. He had difficulty tolerating wound care pain with traditional opioids alone and showed dramatic drops in pain ratings during VR compared to the video game (e.g. a 47 mm drop in pain intensity during wound care). We contend that VR is a uniquely attention-capturing medium capable of maximizing the amount of attention drawn away from the 'real world', allowing patients to tolerate painful procedures. These preliminary results suggest that immersive VR merits more attention as a potentially viable form of treatment for acute pain.

531 citations

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"Novel Object Test: Examining Nocice..." refers background in this paper

  • ...Responses to novel or unfamiliar objects are not only characterized by behavioral aversion but also by potentially detrimental, aversive physiologic responses.(5,26,30,54,76) These reactions have been shown to be comparable to threatening situations....

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Frequently Asked Questions (9)
Q1. What is the effect of morphine on fish?

Intramuscular injection of morphine had a significant analgesic effect in the acid-injected fish by substantially reducing nociception-related behaviors and respiration rate, as well as returning the fear responses to a novel object to normal. 

Other animal studies have shown that exposure to novelty and predators can evoke a stress analgesia with a total reduction in pain reactivity. 

In the novel object test in which the fish’s attention is dominated by the noxious stimulation, it might be that the OBR does not increase after object presentation because little attention and neural processing can be diverted to this physiologic response. 

Although the animals experiencing noxious stimulation did not show fearrelated avoidance behavior, they did show reduced nociception-related behaviors, rocking and rubbing, compared with the frequency of these behaviors before presenting the object. 

16 Comparative genetic studies have shown that the opioid receptor family hasbeen highly conserved during evolution, with fish opioid receptors having 91% similarity with human opioid receptors. 

the 30-minute recovery period after morphine injection is likely to be sufficient time for the analgesic to have diffused into the blood and body tissues. 

46 Relatively little is known about the effects of endogenous opioids in fish, although enkephalins and β-endorphins are present in fish neurons. 

Novel object presentation was repeated an additional 4 times at hourly intervals, and at each presentation a differently shaped and colored novel object was used. 

In this study nociception-related behavior affected fear responses, and one interpretation is that this noxious treatment might command the majority of the attention capacity in fish subject to this experimental situation.