A rebuttal to the paper: “Do fish have nociceptors: Evidence for the evolution of a vertebrate sensory system” published in Proceedings of the Royal Society, 2003 by Sneddon, Braithwaite and Gentle.

By Professor James D. Rose

The paper by Sneddon et al is deeply flawed and does not provide any legitimate evidence that trout are capable of feeling pain. There are numerous problems with methods and interpretation in this paper, but this critique will focus only on those of greatest significance.

The behavioral studies of rainbow trout were done by injecting of relatively large volumes of one of three solutions (bee venom, acetic acid solution or dilute sal****er) into the jaw of rather small trout. For the sizes of the fish used, this injection of liquid would have been equivalent to 100 millilitres (more that 3 ounces) of solution into the lip of a human weighing between 30 and 100 kilograms (66 to 220 pounds). Bee venom contains a great variety of toxins that affect the nervous system and cause a hormonal stress response in addition to stimulating nociceptive receptors signaling tissue injury.

In spite of the massive dose of venom or acid, the activity level of these fish was not affected, they did not hide under a shelter in the tank and they resumed feeding in less than three hours. The acid and venom-injected fish did show a rocking behavior that is likely to reflect a difficulty of the fish maintaining an upright posture, given the magnitude of the toxic chemical trauma created by the injection, rather than an indication of “pain”.

The most impressive thing about the result of the acid and venom injections was the relative absence of behavioral effects, given the magnitude of the toxic injections. How many humans would show little change in movement or be ready to eat less than three hours after getting a lemon-sized bolus of bee venom or acid solution in their lip? Rather than proving a capacity for pain, these results show a remarkable resistance to oral trauma.

It comes as no surprise, then, that many anglers have had the experience of catching the same fish repeatedly within a span of a few minutes. Of course predatory fishes, including trout, feed avidly on potentially injurious prey like crayfish, crabs and fish that have sharp spines in their fins – which further indicates that these fish are not highly reactive to oral noxious stimuli.

Another serious issue of interpretation is that the authors of this paper used an invalid standard for attempting to identify pain. This paper does not actually deal with pain (a conscious experience). It deals only with nociception (unconscious responses to noxious stimuli). I have already addressed the kinds of conceptual confusions that undermine the paper by Sneddon et al in my 2002 Reviews in Fisheries Science Paper, which they did not cite.



The flaws in their argument include the following:-

(1) Their definitions of pain and nociception are invalid and misleading. Pain, as defined by the International Association for the Study of Pain, is purely a conscious experience, with a sensory component and a component of emotional feeling (suffering). In contrast to this conscious experience of pain, the detection, processing and transmission of information related to injury by lower, subcortical, levels of the nervous system is unconscious and defined as nociception – not pain. According to Sneddon et al any behaviour that is a reflex would be evidence of nociception, but any behavior more complex than a reflex would be evidence of pain.

This way of distinguishing pain from nociception is invalid because there are clearly complex, non-reflexive behaviors that can be purely nociceptive and unconscious. For example, humans with extensive damage or dysfunction of the neocortex in the cerebral hemispheres can still make a complex of responses including facial displays, vocalizations, struggling and avoidance reactions to nociceptive stimuli, but they are unconscious and unable to experience pain. By the definition of pain used by Sneddon, et al. it would be concluded that these unconscious humans are feeling pain rather than making purely nociceptive responses, which is clearly erroneous.

There are many other examples of complex, non-reflexive behaviors that can be performed unconsciously, like the fact that sleepwalkers can open doors, navigate around obstacles and speak while unconscious during deep sleep.

(2) Most important – in order to show that a fish (or any organism) experiences pain, it is necessary to show that a fish has consciousness. Without consciousness, there is no pain. Nothing presented in this paper necessitates predication of consciousness for its explanation and the authors don’t even deal with this essential issue. Furthermore, as I have shown in my 2002 Reviews in Fisheries Science paper there is extensive scientific evidence showing that pain and consciousness depend on very specific brain regions, namely specialized neocortical regions of the cerebral hemispheres. These brain regions are absent in fishes and there are no likely alternative brain systems to perform the same functions. Consequently, there is no basis for assuming that a fish might have a capacity for consciousness or pain.

The burden of proof that trout are conscious and potentially capable of feeling pain remains on these authors and they have ignored this issue by citing previous studies that also used invalid criteria, such as a capacity for avoidance learning (which actually occurs unconsciously) for demonstrating pain. Only anthropomorphic speculation would lead one to conclude that the trout in this study are experiencing pain.



The evidence that Sneddon et al present for nociceptive sensory receptors in trout is neither wholly original nor unexpected. In my 2002 Reviews paper, I cited a much earlier paper, published by Whitear in 1971, that showed the presence of C-fibers in bony fishes (e.g. fishes like trout). C-fibers are a principal type of nociceptive receptor.

The bottom line is that any attempt to show pain in fish must use valid criteria, including proof of conscious awareness in fish. This is not something that can be taken for granted, because on neurological and behavioral grounds it is so improbable that fish could be conscious and feel pain. We know a great deal about the neurological requirements for consciousness and the experience of pain. Extensive, specialized regions of neocortex are required. Fish lack these brain regions and have no likely substitute systems for performing the same functions. Furthermore, the behavioral results of this study show that in spite of very large injections of acid solution or venom, the fish showed relatively little adverse effects.

The improbability that fish can experience pain in no way diminishes our responsibility for concern about their welfare, because they are still capable of robust behavioral, physiological and hormonal responses to stressors, which if sufficiently sustained, can be detrimental to fish health. But, extensive factual evidence makes it extremely improbable that fish are capable of experiencing pain or suffering.

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Cited reference: Rose, J. D. 2002. The neurobehavioral nature of fishes and the question of awareness and pain. Reviews in Fisheries Science, 10: 1-38. This paper can be obtained from the author in electronic form from his website:
http://www.uwyo.edu/Zoology/faculty/rose/ (*)


James D. Rose, Ph.D.
Department of Zoology and
Physiology
University
of Wyoming
Laramie, WY 82071
USA

trout@uwyo.edu

2nd May 2003

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