What’s it feel like to be a fish? I contend that it doesn’t feel like anything to be a fish. Interestingly, much of our own lives are led without attending to how we feel. We just get on with it and do things. Most of the time we act like automatons. We manage to get dressed in the morning, or walk to the bus station, or get in the car and drive to the shops without thinking about what it feels like. Consequently, much of what we do is accomplished non-consciously.
There is an enormous amount of neural processing of information in the brain that never reaches our consciousness (that is, we never become aware of it and hence are unable to report it). I propose that fish spend all of their lives without ever feeling anything. In a recent paper in the academic journal Biology & Philosophy (Key, 2015) I discussed this idea in relation to the feeling of pain. I argued (as have others; Rose et al., 2014) that there is no credible scientific evidence for fish feeling pain.
I will now address the question about whether fish feel pain in this article using a slightly different approach. I propose that by defining how the human brain processes sensory stimuli in order to feel pain, we will be able to define a set of minimal neural properties that any vertebrate must possess in order to, at least, have the potential to experience pain. As an introduction to this argument I first highlight anthropomorphism as a major stumbling block for many people in recognizing fish do not feel pain and then I discuss the difference between noxious stimuli and pain since these terms are often conflated.
Resisting anthropomorphic tendencies
Grey wolves hunt as a pack. They carefully select their prey, and then perform a series of highly coordinated maneuvers as a team, in order to corral their target. Initially, each wolf maintains a safe working distance from other members of the pack as well as from their prey. They are relentless and seemingly strategic with an overall goal of driving the agitated prey towards one wolf. A cohesive group mentality emerges that portrays logic, intelligence and a willingness to achieve a common goal. Eventually one wolf comes close enough to lock its jaws on a rear leg of the prey, before wrestling it to the ground. The rest of the pack converges to share in the kill. There appears a purpose to their collective behavior that ensures a successful outcome.
But is everything as it seems? A team of international scientists from Spain and the U.S.A. has simulated the behavior of a hunting pack of wolves using very simple rules (Muro et al., 2011; Escobedo et al., 2014). Their computer models do not rely on high-level cognitive skills or sophisticated intra-pack social communication. The complex spatial dynamics of the hunting group emerges by having the computer-generated wolves obey simple inter-wolf and wolf-prey attractive/repulsive rules.
For instance, much of the hunting strategy can be reproduced by having each simulated wolf merely move towards a prey while keeping a safe distance from it and other wolves. In this way the prey is driven towards a single wolf in the pack. Simple rules are all that are needed to generate this hunting behavior. There is no need for sophisticated communication between the wolves, apart from visual contact. There is no need for a group strategy, each wolf can act independently to create what appears to be an elaborate ambush.
The lesson is clear. Watching and analyzing animals behaving, either in the wild or in captivity, is fraught with tendencies to describe underlying causes of actions and reactions in terms of human experience. This human-centered explanation of behavior is referred to as anthropomorphism: when humans observe animals responding to a sensory stimulation in a way that reflects how they would react, there is often a strong desire to invoke anthropomorphic explanations.
One can easily imagine that a group of humans closing in on a prey would either communicate amongst themselves or learn from experience how each other is thinking, and hence how they would react to different scenarios in order to achieve a common goal. Because humans so easily reflect on their own behavior, human-like qualities are bestowed on animals spontaneously. For example, when a fish squirms after it is hooked, there is a natural tendency to imagine the pain that the fish is feeling. It seems intuitive. A hook in your mouth would hurt, so why wouldn’t fish feel the same.
Our anthropomorphic and sometimes intuitive view of the world is not, however, always helpful in understanding the behavior of animals (particularly those that are not our close relatives; de Waal, 2009). Yet, even scientists at the top of their profession adopt anthropomorphism, a line of thinking that can camouflage biologically and evolutionarily more plausible explanations of animal behavior. (However, not everyone will agree. Readers are referred to an essay by Marc Bekoff; Bekoff, 2006).
Why do humans so easily fall victim to anthropomorphism? One could argue that we are hard wired for empathy and hence anthropomorphism, especially given the role of a specialized set of neurons in the cortex (so-called mirror neurons) and subcortical regions which appear to non-consciously drive these behaviors (Corrandini and Antonietti, 2013; Gazzola et al., 2007; Heberlein and Adolphs, 2004).
Defining key terms
One of the common queries raised by discerning readers is that if fish don’t feel pain, why do they then squirm, flap and wriggle about in distress when they are raised out of water? Why do they fight so hard to escape a fisherman’s line? It is a simple and emotionally powerful anthropomorphic argument. That is, if a hook was pierced into your lips and then someone yanked on it, wouldn’t you struggle to escape and free yourself, just like a fish?
Maybe not. A wild horse submits to a leash within minutes. A bear trapped in a foot snare shortly gives up its struggle. Why does a fish continue to fight in the face of supposedly extreme pain (in some cases, as in big-game sport fishing, fish will relentlessly fight against the hook for 1-2 hours). An alternative view is that fish do not feel pain.
There are two terms that need defining here: fish and pain. When I refer to fish, I am referring only to bony ray-finned fish, since they are the most common experimental fish model and the fish most people are familiar with (these are fish with bones as well as fins that have spikes). The most defining anatomical feature of ray-finned fish is gills. Whales, porpoises, dolphins, seals, otters and dugongs are not fish. These animals are marine mammals; they possess lungs rather than gills.
Pain is a term that many readers will not have difficulty in understanding. Everyone has some vivid recollection of it, after touching something hot or smashing a thumb with a hammer. However, we must be very clear in our definition given the claim that fish do not feel pain. Pain is the subjective and unpleasant experience (colloquially referred to as a “feeling”) associated with a mental state that occurs following exposure to a noxious stimulus.
The mental state is the neural activity in the brain that is indirectly activated by the stimulation of peripheral sensory receptors. A noxious stimulus is one that is physically damaging to body tissues (e.g., cutting, cold and heat) or causes the activation of peripheral sensory receptors and neural pathways that would normally be stimulated had the body been physically damaged.
Gentle touch and warm water are not noxious stimuli. They neither cause physical damage to tissues nor activate sensory receptors and nerves normally stimulated by physical damage. It should be noted that pain is not a necessary consequence of noxious stimuli. For example, there are many anecdotes of people who have experienced traumatic accidents resulting in severe body tissue trauma without feeling any immediate pain. This means that it is possible to cut your skin without feeling pain.
Some basic neurobiological concepts
To feel pain requires that you are aware or conscious of your own mental state. To be aware first requires that you attend to the stimulus. A simple demonstration of this concept is illustrated by asking you to feel the pressure on your ischial tuberosities (the bony parts of the pelvis that you sit on) when you are seated. Before I directed your attention to your backside you were probably not aware of it, but immediately afterwards you became conscious of the feeling of your seated position. To feel a sensory stimulus requires attention to that stimulus (in this case, pressure on the ischial tuberosities).
Awareness of the mental state associated with peripheral stimulation of sensory receptors arises as a result of the process of attention. This is called the top-down attentional system since it involves the frontal lobes, supposedly the highest hierarchical level in the brain (Collins and Koechlin, 2012). However, attention is not always under conscious or voluntary top-down control. It is possible for the sensory stimulus itself to non-consciously activate attentional processes in what is referred to as the bottom-up attentional system (Driver and Frackowiak, 2001). A relevant and simple example would be to accidentally stand on a sharp object while walking. In this case the noxious stimulus activates attentional circuitry and causes awareness (pain, in this example). In humans, the cerebral cortex in the frontal and parietal lobes of the brain is intimately involved in attending to input from our sensory receptors. In summary, feeling pain requires the activity of neural circuits associated with attention. Once the brain is attending to a sensory stimulus then it becomes possible to subjectively experience a specific sensation.
These top-down and bottom-up attentional mechanisms are not specific to feeling pain. Much of our understanding of their contribution to processing of sensory stimuli comes from the visual system (Corbetta and Shuklman, 2002; Buschman and Miller, 2007). What is pertinent to our discussion is that both the top-down and bottom-up attentional mechanisms are dependent on specific neural activity in the frontal and parietal areas of the cerebral cortex, respectively.
What is the cerebral cortex?
In everyday language the cerebral cortex is the “grey matter.” This grey matter is a thin outer covering of the mammalian brain that typically consists of 3-6 discrete horizontal layers of neurons and their processes. These layered neurons are interconnected vertically to create minicolumns or canonical microcircuits that are repeated across the whole surface of the brain. Each of these minicolumns is interconnected horizontally to produce a massively powerful processing machine.
These canonical microcircuits can be likened to integrated circuits or microprocessor chips in computers. As computers have evolved, more and more circuits have been added to their chips (you may remember the progression in personal computer evolution from 286 to 386 to 486 to Pentium and Core chips). The cerebral cortex has evolved by both increasing the complexity of the canonical microcircuit from 3 layers to 6 layers of neurons (the latter is called the neocortex) and by adding more and more of these “chips,” leading to an expanded surface area of the cortex (Rakic, 2009).
Pain is in the cerebral cortex
Pain causes elevated electrical activity in at least five principal regions in the human forebrain: the anterior cingulate cortex (ACC), the frontal and posterior parietal cortex, the somatosensory (S) regions I and II, the insular cortex, and the subcortical amygdala. These five regions form a core, interconnected circuit that is referred to as the pain matrix (Brooks and Tracey, 2005).
However, just because there is electrical activity in a particular brain region during pain does not mean that that region is responsible for the sensation. For example, while the amygdala is active during pain it is involved in modulating the pain (as well as many other things), rather than producing the feeling of pain. This has been clearly demonstrated in ablation studies in both rats and rhesus monkeys. These animals continue to quickly remove their tails away from a noxious heat stimulus even after bilateral ablation of their amygdala (Manning and Mayer, 1995; Manning et al., 2001; Veinante et al., 2013). Consequently, it is reasonable to remove this subcortical region from the matrix responsible for feeling pain.
On this criterion, the ACC also does not belong to the feeling-pain matrix. Lesion of the nerve fibers arising from the ACC is called cingulotomy and has been practiced clinically for over 50 years to relieve intolerable pain. However, patients continue to feel pain after this surgery — they just no longer seem to be bothered by the presence of their pain (Foltz and White, 1962). Thus, the ACC is not responsible for feeling pain per se. The frontoparietal nexus is likewise associated with attention to pain rather than the actual feeling of pain (Lobanov et al., 2013).
There is compelling evidence that SI, SII and the insular cortex are the essential components of the pain experience. For example, there is an interesting clinical case of a patient who had ischemic stroke that selectively damaged a small portion of SI and SII in the right side of the brain (Ploner et al., 1999). This patient could no longer perceive any acute pain in response to thermal noxious stimuli or pinprick to the left hand (Ploner et al., 1999). In addition, numerous other clinical studies have revealed that when cortical lesions involve a substantial portion of SI, patients no longer experience any pain (Vierck et al., 2013). Likewise, patients with lesions to the SII-insula cortex have been shown to either lack the sensation of pain (Biemond, 1956) or have altered pain perception (Starr et a., 2009; Veldhuijzen et al., 2010; Garcia-Larrea, 2012a and 2012b).
Another important test of whether a brain region is responsible for pain is to selectively stimulate that region with electrical current.There are only two cortical regions that have ever been shown to cause pain when electrically stimulated (Mazzola et al., 2012): the SII and the insula, which make these two regions the most critical components of the feeling-pain matrix (Garcia-Larrea, 2012a, 2012b).
What does conscious processing of noxious stimuli involve?
I have already described above that the brain must have attentional mechanisms in order to feel pain. But what else does the brain need to do in order to experience pain? Since pain is, by its very definition, the conscious processing of neural signals arising from noxious stimuli, we should, in the first instance, be asking what does conscious processing in the human brain do. Ideally, if we can identify what conscious processing accomplishes, we should be able to relate this to specific neural architectures. Once these architectures are characterized they can then be used as biomarkers for the likelihood that a nervous system feels pain.
Conscious processing is dependent on at least two non-mutually exclusive processes: signal amplification and global integration over the cerebral cortex (Dehaene et al., 2014). Why are these processes so important? Amplification provides a mechanism to increase signal-to-noise ratio and to produce on-going neural activity after the initial sensory stimulus has ceased (Murphy and Miller, 2009). Global integration ensures the sharing and synchronization of neural information so that the most appropriate response is generated in the context of current and past experiences.
Recently, the amount of information transferred across distant sites within the cortex has been quantified using electroencephalography. These quantitative values have been successfully used to distinguish between conscious, minimally-conscious and non-conscious patients (Casali et al., 2013; King et al., 2013). Thus, global integration is a critical defining feature of conscious processing.
What neural architectures enable the cortex to perform signal amplification and global integration? Both of these processes rely on the global propagation of neural information over the cortex surface. Such propagation is achieved by extensive lateral interconnections (axon pathways) between cortical regions. These cortical regions must be reciprocally linked by axons transmitting both feedforward excitatory and feedback excitatory and inhibitory activities (Douglas, 1995; Ganguli et al., 2008; Murphy and Miller, 2009).
In the sensation of pain, amplification involves long-distance attentional pathways associated with the fronto-parietal cortices and their interconnections with the feeling-pain matrix (Lobanov et al., 2013). The SI and SII sensory cortices possess topographical maps of the body that process information associated with the somatosensory system (see Key, 2015). Slight offsets of these maps (at least in human SI) for different sensations has been proposed to allow integration of different qualities (e.g,. touch and nociception: Mancini et al., 2012; Haggard et al., 2013).
This idea has gained considerable support from recent high resolution mapping in primates (Vierck et al., 2013). It is now clear that different sub-modalities of pain, such as sharp-pricking pain and dull-burning pain, are mapped in different subregions of SI. Moreover, lateral interactions between these subregions significantly alter their relative levels of neural activity (Vierck et al., 2013).
Somatotopic maps of noxious stimuli also exist in the anterior and posterior insular cortex (Brooks et al., 2005; Baumgartner et al., 2010). Separate somatotopic maps are present for pinprick and heat noxious stimuli within the human anterior insular cortex (Baumgartner et al., 2010). This segregation of sensory inputs raises the possibility that integration occurs between these two sub-modalities and also allows these sub-modalities to be integrated separately as well as together with emotional and empathetic information that reaches the anterior insular cortex (Damasio et al., 2000; Baumgartner et al., 2010; Gu et al., 2010; Gu et al., 2013; Frot et al., 2014).
Amplification and global integration is also dependent on the local microcircuitry in each cortical region (Gilbert, 1983). The local cytoarchitecture of the cortex (the presence of discrete lamina and columnar organization) is capable of simultaneously maintaining both the differentiation and spatiotemporal relationships of neural signals. For example, separate features or qualities of sensory stimuli can be partitioned to different lamina while the columnar organization enables these signals to be integrated. Both short- and long-range connections between columns provide additional levels of integration.
The six-layered neocortex is well suited for this neural processing. Signals from the thalamus terminate in layer 4 and are then passed vertically to layer 2 within a minicolumn. Activity is then projected to layer 5 within the same minicolumn. Strong inhibitory circuits involving interneurons refine the flow of information through this canonical microcircuit (Wolf et al., 2014). The layer 2 neurons project to other cortical regions (local and long-distance), while layer 5 neurons project to subcortical regions.
Taken together, if the signal is strong enough and if sufficient information is transferred and integrated, then the feeling of pain emerges (at present, how this occurs remains a mystery).
In summary, to the best of our knowledge, for any vertebrate nervous system to feel pain it must be capable of transferring and integrating a certain level of neural information. I contend that such a nervous system must have, at least, the following organizational principles:
1. An attentional system to amplify neural information;
2. Distinct topographical coding of different qualities of somatosensory information;
3. The integration of different somatosensory information both between modalities (e.g., touch and pain) and within a single modality (sharp versus dull pain);
4. Higher-level integration of noxious signaling with other relevant information (e.g., emotional valence). This requires significant long-range axonal pathways (feedforward and feedback) between brain regions integrating this information;
5. Laminated and columnar organization of canonical neural circuits to differentiate between inputs and to allow preservation of spatiotemporal relationships. The lamina must be capable of processing inputs as well as outputs to either higher or lower hierarchical regions while maintaining meaningful representations of the neural information. The lamina must possess strong local inhibitory interneuron circuits to filter information;
6 Strong lateral interconnections (both local and long distance) between minicolumns to maintain integrity and biological relevance of processing in relation to initial stimulus.
I propose that each of these features is necessary but not sufficient for pain in vertebrates. On this basis it should be concluded that fish lack the prerequisite neuroanatomical features necessary to perform the required neurophysiological functions responsible for the feeling of pain. Fish lack the distinct topographical coding of spatiotemporal integration of different somatosensory modalities; they lack the higher–order integration of somatosensory information with other sensory systems; and they lack a laminated and columnar organization of somatosensory information. What, then, does it feel like to be a fish? The evidence best supports the idea that it doesn’t feel like anything to be a fish. They are non-conscious animals that survive without feeling; they just do it. There is nothing heretical about this idea. For much of our lives, we humans also exist non-consciously.
Brian Key is a Professor of Developmental Neurobiology in the School of Biomedical Sciences, University of Queensland. He is the Head of the Brain Growth and Regeneration Lab there. The Lab is dedicated to understanding the principles of stem cell biology, differentiation, axon guidance, plasticity, regeneration and development of the brain.
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