Hide table of contents

Executive Summary

In this, the final of three posts on features potentially relevant to invertebrate sentience, we assess 9 learning indicators, 4 navigational skills, and 7 mood state behaviors. Here are some high-level takeaways:

  1. Simple learning abilities, such as classical conditioning, sensitization, and habituation, do not appear to be good evidence of sentience.
  2. Contextual learning and long-term behavior alteration to avoid noxious stimuli are better evidence of sentience.
  3. It’s plausible that the evolutionary role of consciousness is to produce an integrated and egocentric spatial model of the world to guide an animal as it navigates a complex environment.
  4. It’s difficult to study emotions in invertebrates.
  5. Notwithstanding (4), it appears there are striking behavioral and neurochemical similarities between mammalian responses to stressful stimuli and the responses of certain arthropods.

Introduction and Project Overview

This post is the fifth in Rethink Priorities’ series on invertebrate[1] welfare. In the first post we examine some philosophical difficulties inherent in the detection of morally significant pain and pleasure in nonhumans. In the second post we discuss our survey and compilation of the extant scientific literature relevant to invertebrate sentience,[2] as well as the strengths and weaknesses of our approach to the subject. In the third post we explain some anatomical, evolutionary, and behavioral features potentially indicative of the capacity for conscious experience in invertebrates. In the fourth post we explain some drug responses, motivational tradeoffs, and feats of cognitive sophistication potentially indicative of the capacity for conscious experience in invertebrates. In this post we explain some learning indicators, navigational skills, and mood state behaviors potentially indicative of the capacity for conscious experience in invertebrates. In the sixth, seventh, and eighth posts, we present our summary of findings, both in narrative form and as an interactive database. In forthcoming work, to be published in late July, we analyze the extent to which invertebrate welfare is a promising cause area.

Learning Indicators

Classical conditioning

Also known as respondent or Pavlovian conditioning, this features refers to an organism learning to make an association between an unconditioned, inherently rewarding or punishing stimulus, and another, often neutral, stimulus. The prototypical example of this feature is a dog learning to salivate in response to a bell that has been used to signal the arrival of food. This feature is one of the most basic forms of learning.

Allen et al. 2009 demonstrates classical conditioning in the severed spinal cord of a rat exposed to shocks, thus showing this ability is possible without any connection to a brain at all.[3] Though intact rats apparently have a greater response to the same stimuli, the fact that this can occur at all without interaction with a brain suggests that observing this behavior in isolation may not be much evidence for the capacity for valenced experience. Additionally, this type of conditioning often operates unconsciously in humans, further undermining its evidential force.[4]

Operant conditioning

Operant conditioning, also known as instrumental conditioning, is a type of associative learning in which the frequency of a particular behavior is increased or decreased by pairing the behavior with a punishment or a reward. Operant conditioning differs from classical conditioning in that operant conditioning governs voluntary behavior and classical conditioning governs involuntary behavior. For example, in a laboratory setting a rat might be trained to depress a lever by pairing depression of the lever with a food pellet. Conversely, the rat might be trained to avoid the lever by pairing lever contact with an electrical shock. Pressing a lever to receive a food reward is a voluntary action. However, if the rat began to salivate at the sight of the lever, that would indicate that it had been classically conditioned as well, because salivation is involuntary.

Operant conditioning is a basic form of learning and is widely observed throughout the animal kingdom. Most forms of behavior alteration require at least an element of operant conditioning. Any time an organism learns a new action or learns to perform an old action differently, operant conditioning is probably at work. Thus, we should only expect organisms whose behavior is completely hardcoded or innately determined to lack this feature.

In addition to mere operant conditioning, we also investigated operant conditioning with an unfamiliar action. An organism satisfies this feature just in case it is capable of being operantly conditioned to perform an action it would not perform in its natural environment, such as depressing a lever. Operant conditioning with an unfamiliar action demonstrates some degree of behavioral plasticity and thus is slightly better evidence for conscious experience than mere operant conditioning.


Sensitization is a type of non-associative learning in which an organism amplifies its response to a stimulus, often a noxious stimulus, as a result of repeated exposure to the stimulus.[5] The classic example of sensitization was studied in the sea hare Aplysia californica.[6] If an electric shock to the tail is paired with a touch to the siphon, the sea hare will withdraw its gill. After sensitization has been established, even a light touch of the siphon will initiate a rapid gill withdrawal.[7] Sensitization is one of the most basic forms of learning. It has been demonstrated in the nematode Caenorhabditis elegans[8] and the unicellular protist Spirostomum.[9] As such, possession of this feature probably does not constitute much evidence for the capacity for valenced experience.


Habituation is a type of non-associative learning in which an organism becomes accustomed to a stimulus. Organisms which are habituated to a given stimulus take longer to respond to the stimulus and ultimately may not react to the stimulus at all. Habituation occurs when an organism is frequently exposed to a stimulus, such as a loud noise, with no biological consequence.[10] An animal might initially react to a loud noise with a startle response, but if the loud noise is repeated frequently and without additional consequence, the startle response will begin to weaken and eventually disappear altogether. Habituation has been observed in some species of plant[11] and even single-celled organisms,[12] and in humans, it is an automatic, unconscious response.[13] Thus, habituation probably involves relatively simple mechanisms and does not provide much evidence of consciousness.

Contextual learning

Contextual learning is the ability to discriminate between different contexts in a sophisticated way. More formally, contextual learning is “learning that in context 1 stimulus A is rewarded while stimulus B is not (AC1+ and BC1−), whereas it is the opposite in context 2 (AC2− and BC2+).”[14] For example, honey bees are capable of multimodal associative learning. They can recognize that when one color is presented to them, odor A predicts a sucrose reward and odor B does not, but when a different color is presented odor B predicts a sucrose reward and odor A does not.[15] (This finding reflects the fact that when foraging, a single modality by itself can’t parse beneficial flower species from non-beneficial species. Bees rely on a combination of color, shape, and odor to distinguish good flowers from useless ones.) Contextual learning contributes to behavioral plasticity. According to some researchers, behavioral plasticity is a hallmark of consciousness. For example, Paula Droege, a philosopher at Penn State, argues that “animals capable of flexible responses are conscious animals, animals that feel conscious pain.”[16] Animals that cannot engage in contextual learning must rely on behaviors that are more rigid, reflexive, and programmatic.

Observational or social learning

The ability to learn by observing the behavior of one’s conspecifics is widespread in animals. This phenomenon is known as “social learning,” and it stands in contrast to “asocial learning,” in which an animal learns by personal trial and error. The extent to which an animal can learn complex behavior by observing the behavior of others is often taken to be an indicator of cognitive sophistication. Like other forms of learning, social learning is not direct evidence for the capacity for valenced experience. It is rather a rough guide to a certain sort of intelligence. If that type of intelligence is positively correlated with the capacity for valenced experience, and we don’t have reason to think the correlation is spurious, then the presence of social learning in an animal may be indirect evidence that that animal is capable of valenced experience.[17]

Social learning has been demonstrated in invertebrates. Alem et al. 2016 shows that bumblebees are capable of so-called “cultural transmission.” The authors trained bees to pull a string in order to receive a reward. By observing this practice in trained bees, untrained bees acquired the skill. The skill eventually spread to a majority of the colony’s foragers. The skill then persisted in the colony far longer than the lifespans of the initial trained bees.[18]

More so than other features, it must be emphasized that the ability to learn by observation comes in degrees. Great apes are capable of acquiring elaborate novel skills such as termite fishing or potato washing merely by observing and imitating other apes.[19] In other taxa, social learning is less complex and is mediated by relatively simple learning mechanisms. Thus, it is important to understand the precise nature of the social learning in question before one can judge how it bears on the issue of valenced experience.[20]

Taste aversion behavior

Taste aversion is a type of behavior in which an organism exhibits ‘disgust responses’ to a particular flavor. In humans disgust responses include retching, clutching at the stomach, and vomiting. Disgust responses vary among nonhumans. Rats, which are incapable of vomiting,[21] display disgust by gaping, chin rubbing, and paw treading.[22] Chickens putatively display disgust by head shaking and beak clapping.[23] Cuttlefish will quickly release a food source coated in quinine (a bittering agent) and withdraw to a corner of their tank, which has been interpreted as a disgust response.[24]

Taste aversion is importantly distinct from taste avoidance. Taste avoidance occurs when an organism consumes a smaller amount than usual of a food with a certain taste. The levels of the two phenomena can vary independently of each other. For example, some organisms will consume large amounts of a substance that has a psychoactive effect even if they show signs of nausea while consuming it. Similarly, an organism might avoid a particular taste even if the taste does not make it nauseous, such as when that taste is associated with a fearful event.[25]

Taste aversion is potentially important because disgust behavior, like pain behavior, is modest evidence of valenced experience. A natural explanation of disgust behavior is that the organism exhibiting the behavior experiences a negatively valenced gustatory sensation. In the absence of defeaters, such an explanation is to be preferred to alternative explanations.

One obvious barrier to using taste aversion as evidence for valenced experience is that it is not always clear what constitutes a disgust response. Even where it exists, our ability to detect taste aversion may be limited by anatomy. For example, insects have hard exoskeletons, and so they are not be able to form facial expressions associated with nausea or disgust.[26] Conversely, what looks like a disgust response in vertebrates may be something else entirely in invertebrates. Flies and other insects routinely vomit on food as a form of extra-oral digestion. The vomit contains digestive juices and enzymes that help liquefy the food, making feeding easier, but it is not a disgust response.[27]

Pain-relief learning

Pain-relief learning is a type of associative conditioning in which the subject comes to associate the stimulus that immediately follows a noxious event with relief from the aversive effects of the noxious event.[28] (Importantly, pain-relief learning is not merely a type of operant conditioning in which an organism learns a specific active response that relieves pain.) In an electric shock paradigm, if a stimulus, such as an odor or tone, is consistently experienced just prior to the shock, eventually the stimulus alone will induce a negatively valenced state. The opposite is also true. If a stimulus is consistently introduced just after the shock, that stimulus alone will eventually acquire a positive valence due to its association with the relieving cessation of pain. This phenomenon is well-documented in humans, rats, and, crucially, fruit flies.[29] Fruit flies are able to distinguish cases in which a stimulus precedes a noxious event from cases in which a stimulus follows a noxious event. Indeed, fruit flies can be systematically conditioned to either avoid or approach an odor merely by altering the timing of the release of the odor relative to an electric shock.[30]

An organism that did not satisfy this feature would seem to either have a reward system that differed from ours in important respects or to have an affective or cognitive system not complex enough to register the association. Differences in reward systems weakens the analogy between other conscious animals and these beings, and so this would represent evidence against them being conscious.

Long-term behavior alteration to avoid noxious stimuli

Some short-lived animals are so well-adapted to their evolutionary and ecological niche that automatic, instinctive responses alone are sufficient to keep the animals safe from harm. Animals in more complex situations (either ecologically or socially) need more plastic responses to keep them safe. One evolutionary function of conscious pain experiences—perhaps the evolutionary function of conscious pain experiences—is to promote long-term bodily integrity through behavior modification. Although not all damaging injuries are painful and not all pain experiences result from damaging injuries, there is nonetheless a fairly tight correlation between tissue damage and pain sensation. This correlation allows animals to learn from pain experiences. Sneddon et al. 2014 argues that the “key function [of pain] appears to be that the aversive experience of pain creates a strong and lasting motivation that enables the animal to avoid getting into a similar situation in the future.”[31]

Mere nociception is unlikely to be an efficient response to noxious stimuli in the long-term. Nociception is fast and reflexive, but it is not normally associated with a lasting memory. On the other hand, conscious pain experiences, with their attendant felt badness, tend to leave a memorial imprint.[32] Because pain experiences are often stored in long-term memory, pain can induce long-term behavioral and motivational changes. For long-lived animals in complex environments, pain is potentially more effective at protecting the animal from damage than mere nociception. Again in the words of Sneddon et al. 2014: “while nociception typically allows for an immediate reduction of tissue damage, pain typically allows for longer-term protection.”[33] Thus, insofar as invertebrates exhibit long-term behavior alterations in response to noxious stimuli, that is evidence that they experience the noxious events as painful.

Unfortunately, the evidential status of long-term behavioral alteration has recently been complicated by new studies of nociceptive systems. Such systems can be enormously complex, and in some instances nociceptive systems exhibit a degree of plasticity. For example, Smith and Lewin 2009 discuss the process of nociceptive sensitization, a phenomenon that “manifests as either non-responsive neurons becoming responsive, or neurons responding at reduced threshold and/or producing responses of greater magnitude.”[34] If nociception can produce long-lasting effects without the involvement of conscious experience, then the evidential weight of long-term behavioral alteration is undercut.

Note also that “long-term” is a predicate that comes in degrees. Furthermore, what counts as a “long-term” behavior modification is plausibly relative to the lifespan of the creature modifying its behavior. For lifespans measured in weeks, remembering a phenomenon for several days may confer the same fitness advantage as a longer-lived creature remembering a phenomenon for months. Thus, what qualifies as “long-term” for a fruit fly may not qualify as “long-term” for a cow. In response to these problems, we have introduced two versions of this feature. The first measures whether behavior alteration persists more than 24 hours. The second measures whether behavior alteration persists more than 30 days. We realize this is an imperfect solution to the problem, but given our constraints, it was the best we could do. When an animal clearly exceeds the 24 hour threshold but falls just shy of the 30 day threshold (as is the case with sea hares), we have noted as much in the comments.

An organism possesses this ability if it can navigate to a destination within an area that is already known to the organism. This is a very basic navigational skill, exhibited by most motile animals, some amoeboid protists,[35] and many robots.[36] As such, possession of this ability does not provide much evidence for the capacity for valenced experience.

An organism possesses this ability if it can navigate to a destination within an area that is unknown to the organism. In general, navigational skills are relevant for the detection of valenced experience in virtue of their possible connection to conscious experience more generally. According to some researchers, the evolutionary function of consciousness is to produce an integrated and egocentric spatial model to guide an animal as it navigates a complex environment.[37] If consciousness evolved specifically to aid motile animals in complex environments, then various navigational feats could plausibly be interpreted as evidence of consciousness in evolved creatures.

There is at least circumstantial evidence that navigating novel environments requires conscious input whereas navigating known environments does not. In humans, conscious awareness seems to be required to maneuver through the unknown but not the known. Unconscious sleepwalkers can navigate familiar landscapes (moving from the bedroom to the kitchen, say), but they are generally unable to successfully traverse unfamiliar areas.[38]

In laboratory settings the ability to navigate unknown areas is often tested with mazes. The strength of this ability is measured along at least two axes: the efficiency with which the organism can solve a novel maze and the complexity of the maze used in the experiment. However, there may be limits to this methodology. There is a sense in which unicellular slime molds can “solve” relatively complex mazes.[39] It is not clear exactly what to make of this result, or even if it is intelligible to speak of unicellular organisms navigating at all. The slime mold case is a useful reminder that lab results can be interpreted in multiple ways. As is normally the case, evidence for consciousness in one species may not be as compelling for another species.

Spatial memory

Spatial memory is the faculty animals use to return to rewarding locations (e.g., dens, foraging sites, food caches, watering holes, nesting beaches). A variety of different cues can form the basis of this type of memory, including visual or olfactory landmarks, distances, and cardinal directions. Spatial memory has been demonstrated in a large range of animals, including invertebrates.[40] Many species of bee, for example, engage in trapline nectaring: the establishment of regular routes for visiting flowers in a precise repeated order. Other insects engage in patrolling behavior: repeated loops or back-and-forth routes to defend resources from conspecifics.[41] Cephalopods are also known to have a good working memory of recent foraging areas.[42]

Spatial memory is potentially relevant to consciousness because of its relationship to what Michael Trestman, a philosopher of biology at Indiana University, calls a “complex active body” (CAB).[43] A CAB is capable of independent, perceptually-guided, powered-motion (e.g., swimming, flying, crawling). According to Trestman, the evolution of CABs requires the capacity for integrated, embodied spatial cognition, including spatial memory. If one adopts a “global workspace” theory of consciousness, a sophisticated, integrated form of cognition (of which spatial memory forms a part) of this sort is evidence for phenomenal consciousness.

One complication merits discussion. Memory in general, and spatial memory in particular, need not be internal. Many organisms effectively externalize part of their memory by storing and retrieving information about past events in a physical medium outside their bodies. Humans, of course, utilize Post-It notes and iPhones, but external memory is not unique to us. The pheromone trails deposited by many species of ants have been described as a form of external memory.[44] Even very simple organisms, such as the brainless slime mold Physarum polycephalum employ a form of external memory. As the mold moves, it leaves behind a coating of nonliving, extracellular slime. As the mold explores, it tends to avoid contact with the extracellular slime. Reid et al. 2012 reports that this “avoidance behavior is a ‘choice’ because when no previously unexplored territory is available, the slime mold no longer avoids extracellular slime. The slime mold’s behavioral response strongly suggests that it can sense extracellular slime upon contact, and uses its presence as an externalized spatial memory system to recognize and avoid areas it has already explored.”[45] Because it’s not always easy to distinguish external memory from internal memory, we have opted not to make this distinction in our investigations. Thus, according to our methodology, any organism that displays the telltale behavioral indicators of spatial memory counts as possessing this feature, even brainless slime molds. As with many other features, the context in which this ability is observed matters a great deal, and hence the importance of this feature probably ought to be adjudicated on a species-by-species basis.

Detour behavior

Detour behavior occurs when, in order to reach a goal, an organism navigates around a barrier that temporarily blocks sensorial contact with the goal. Detour behavior often requires backtracking, the ability of an organism to retrace its movement. Detour behavior also requires an organism to possess a working memory capable of representing an object outside sensorial contact, retaining that representation over time as the organism moves.[46] Among invertebrates, detour behavior has been observed in jumping spiders,[47] desert ants,[48] and octopuses.[49]

At least some researchers believe that an animal’s navigational skills can tell us something about the organization of that animal’s mind. For instance, Peter Carruthers, a philosopher and cognitive scientist at the University of Maryland, writes, “at least some invertebrates (specifically honey bees and jumping spiders) possess a belief-desire-planning cognitive architecture much like our own, as revealed by their sophisticated navigation abilities.”[50] If it’s true that navigation abilities can provide insight about cognitive architecture, then detour behavior, as the most sophisticated navigational skill systematically studied across diverse taxa, is an important feature to consider.

Mood State Behaviors

Anhedonia behavior

Anhedonia is a loss of interest in activities previously found to be rewarding.[51] In humans, anhedonia is a common symptom of depression. In nonhuman animals, external symptoms of anhedonia may include “behavioral deficits consistent with a loss of responsiveness to reward, such as decreased sucrose consumption, decreased ability to associate rewards with a distinctive environment, and decreased sensitivity to rewarding electrical brain stimulation.”[52] In the absence of defeaters, anhedonia-like behavior in a nonhuman animal is modest evidence that the animal is capable of experiencing a negatively valenced emotional state. Anhedonia-like behavior can be induced in fruit flies by exposing them to aversive, uncontrollable vibrations over several days. The shaken flies show reductions in various voluntary behaviors, although reflexive behavior remains unchanged. In particular, shaken flies consume much less glycerol (commonly used as a reward in fruit fly studies) than non-shaken controls, suggesting that the shaken flies have lost their taste for sweets.[53]

Learned helplessness behavior

Learned helplessness is a condition in which a human or nonhuman animal adopts an overly passive reaction profile that disrupts important voluntary behavior.[54] A creature in the throes of learned helplessness will often neglect basic survival needs, ignoring food, water, predators, and potential mates. Learned helplessness is triggered by repeated, uncontrollable exposure to traumatic stimuli, and it can be reliably reproduced in a number of nonhuman animals. For example, if dogs are subjected to repetitive and unavoidable electric shocks, the dogs will eventually stop trying to evade the shocks, sitting passive and still even if later explicitly given the opportunity to escape.[55] Learned helplessness is a major symptom of depression in humans, and thus the presence of learned helplessness behavior in nonhuman animals is, in the absence of defeaters, modest evidence that those animals are capable of experiencing a negatively valenced emotional state.

One potential defeater is worth flagging right away. Although it may appear that learned helplessness is a relatively sophisticated cognitive condition, the basic characteristics of learned helplessness have allegedly been demonstrated in an isolated ganglion of a decapitated insect. A single cockroach leg connected to its isolated thoracic ganglion can be operantly trained to remain lifted. However, if the leg-ganglion system is subjected to uncontrollable electric shocks before the conditioning, acquisition takes much longer. Summarizing this research, as well as similar research on the severed spines of rats, Eisenstein et al. 1997 reports, “The brain is evidently not essential either in mammals or in invertebrates for demonstrating [learned helplessness].”[56] If that is true, then learned helplessness is almost certainly mediated at least in part by mechanisms much simpler than conscious experience.

Displacement behavior

Displacement behavior is a behavioral response to stress. Common examples of displacement behavior include pacing, fidgeting, grooming, scratching, and object manipulation (such as twirling a pen). Displacement activities are thought to occur when an organism is caught between conflicting motivations. They are thought, and some experimental evidence suggests, to be a ‘comfort’ activity that reduces anxiety in the organism. Displacement behavior often occurs rapidly, incompletely, and out-of-context. For instance, a bird unable to decide whether it ought to flee or attack an opponent might instead quickly preen or peck the ground. Displacement behavior is often exhibited in socially tense situations like these, and in social hierarchies lower-ranking animals exhibit displacement behavior more often than higher-ranking animals.[57] Notably, displacement behavior is increased in a dose-dependent way when an organism is given anxiety-provoking drugs and decreased in a dose-dependent way when an organism is given anxiety-relieving drugs.[58] Displacement behavior is thus modest evidence for the presence of a negatively valenced emotional state.

Displacement behavior has been widely observed in the animal kingdom. Primates (including humans),[59] chickens,[60] and honey bees[61] all display some form of displacement behavior.

Adverse effects of social isolation

A wide variety of animals, both vertebrate and invertebrate, live in groups. These groups range from loose aggregations of ten or fewer animals to massive ant supercolonies containing millions of animals.[62] The adverse effects of social deprivation in group-living vertebrates is well documented. When raised in isolation, such animals are less able to appropriately process social and environmental stimuli. For example, rat pups reared in isolation exhibit a wide range of long-term behavioral and physiological abnormalities, including “neophobia [fear of new things], impaired sensorimotor gating, aggression, cognitive rigidity, reduced prefrontal cortical volume and decreased cortical and hippocampal synaptic plasticity.”[63] Group-living animals display their preference for social contact in a number of ways. Bull calves actively seek out companion animals.[64] Young chicks increase their peeping calls when isolated.[65] The effects of social deprivation in eusocial insects have also been well-studied. Social isolation increases aggression in honeybees[66] and drastically reduces lifespan in ants.[67] More recently, social isolation has been studied in group-living non-eusocial insects. In some species of cockroach, individuals reared in isolation show “stronger exploration-avoidance, reduced foraging activity, reduced willingness to interact socially, and reduced ability to assess mating partner quality compared to peers raised in groups.”[68]

In humans, the adverse effects of social isolation are correlated with negatively valenced emotional experiences. In the absence of defeaters, the presence of similar adverse effects in nonhuman animals is evidence that they experience similar negatively valenced states. Of course, we should not expect animals that do not live in groups to be adversely affected by social isolation. Octopuses, for instance, lead mostly solitary lives and for that reason do not exhibit any noticeable differences when kept in isolation. One should not conclude on that basis that octopuses cannot experience stress from other sources.

Stereotypic behavior

Stereotypies are a type of repetitive behavior that is unvarying and apparently purposeless. Stereotypies are most commonly observed in captive animals. They are usually considered abnormal and are often taken to be evidence of welfare problems. Examples include excessive grooming leading to self-mutilation, swimming in circles, pacing, mouthing cage bars, and chewing without anything in the mouth (so-called “sham-chewing”). Although stereotypic behavior is probably caused by impoverished states, especially situations where the normal functional response of an animal is blocked, stereotypic activities might actually serve to reduce stress, by releasing morphine-like endorphins.[69]

Stereotypic behavior is well documented in captive chickens and cows. Caged hens unable to find or even seek an appropriate nest site engage in stereotypic pacing, while broiler chickens unable to forage engage in stereotypic spot-pecking.[70] Confined cows engage in stereotypic tongue-rolling and often engage in a repeated pattern of getting up and then immediately lying down over long periods of time.

Only recently has stereotypic behavior been observed in invertebrates. Huber et al. 2018 reports that giving crayfish methylenedioxymethamphetamine (MDMA) "triggers repetitive stereotypies in which only the last pair of walking legs stabilizes the body, while all other walking legs, claws, and mouthparts sway back and forth continuously."[71] Andrews et al. 2013 identified stereotypic “pacing” activity in the Giant Pacific octopus, Enteroctopus dofleini, which stopped when environmental enrichment was provided.[72]

According to one estimate, approximately 91% of confined sows, 82% of broiler breeders, and 50% of laboratory mice will engage in some form of stereotypic behavior over a six month period.[73]

Fear/anxiety behavior

All animals react to perceived danger. In humans, one type of reaction to perceived danger is conscious fear. The experience of fear is associated with certain physiological and behavioral responses. Behavioral markings of fear include fleeing, hiding, freezing, and suspending unnecessary bodily functions. Physiological reactions to fear can include elevated heart rate, hyperventilation, increased muscle tension, constriction of blood vessels, nausea, and dizziness. Insofar as other animals display relevantly similar physiological and/or behavioral responses, that is evidence that they too experience conscious fear.

Anxiety is related to but distinct from fear. Anxiety is sometimes said to be the result of danger that is perceived to be unavoidable[74] or situations in which the threat is ambiguous or unknown.[75] Anxiety is often considered a secondary emotion, that is, an emotion in response to another emotion. For example, in humans, generalized fear often leads to anxiety. In addition to physiological and behavioral reactions,[76] anxiety is also associated with certain cognitive changes. For example, anxiety is correlated with pessimistic cognitive biases and generalizability. (In this context, generalizability means that fear or anxiety is not specific to one triggering stimulus; when a creature experiences anxiety, it becomes more afraid of other potential threats as well.[77]) Although the three are phenomenologically and conceptually distinct, fear, anxiety, and pain are all negatively valenced. Thus, the experience of fear or anxiety directly entails the capacity for valenced experience.

Two worries are worth noting with respect to the detection of fear and anxiety in invertebrates. The first is that by applying emotional terms to phylogenetically distant animals, we may be resorting to problematic anthropomorphizing. Both crayfish[78] and honeybees[79] exhibit many of the behaviors associated with human fear and anxiety, but, because those terms come loaded with anthropocentric connotations, applying those terms to those animals may inevitably be misleading.

The other worry runs in the opposite direction. Because the lifestyle and environment of phylogenetically distant animals is so alien to us, we should not expect negative emotional states to be expressed in precisely the same manner. Gibson et al. 2015 reminds us that “distantly related species may express emotion states through behaviors that have no obvious homology to human behaviors.”[80] They advocate for an “alternative approach to identifying instances of emotional expression, which does not depend on anthropocentric homologies” by establishing “general features of emotion states, or ‘emotion primitives,’ which apply both to different emotions in a species and to emotions across phylogeny. One can then search for behaviors that exhibit evidence of such emotion primitives in model organisms.”[81]

Play behavior

Play behavior is difficult to define but easy to recognize. Play behavior is characteristically voluntary, spontaneous, and repetitive (though not stereotypic). Generally only healthy animals in low-stress environments engage in play, and it is most widely observed in juveniles, peaking around puberty. Play behavior is not aimed directly at immediate survival needs or reproduction, but many skills needed for survival and reproduction are practiced during play. Play behavior is commonplace among socially complex animals. It facilitates the acquisition of motor skills, teaches social competence, prepares the animal for unexpected situations, and in general stimulates brain development.[82]

Play is biologically expensive. When playing, animals expend energy, forgo foraging opportunities, and draw (potentially predatory) attention to themselves while in a distracted state. Play behavior even reduces growth rate.[83] Play also appears to be intrinsically pleasurable. Dopaminergic pathways in the brain light up during play. Rat pups ‘chirp’ when playing in the same way as when they are presented with a food reward.[84]

Some researchers believe that play behavior is good evidence for the capacity for valenced experience because, they allege, play behavior plausibly requires the experience of pleasure.[85] Whether or not this is so, play behavior does seem to require a relatively high degree of cognitive sophistication. Play behavior is most common among mammals, and across mammalian orders brain size is positively correlated with playfulness. Play behavior is in general not found in birds, with the exception of the highly intelligent corvid family.[86] Octopuses appear to be the only invertebrate that exhibits play behavior. (Play behavior probably evolved independently in octopuses because the last common ancestor of mammals, birds, and cephalopods almost certainly lacked the cognitive sophistication to engage in play behavior.[87]) Thus, it’s possible that play behavior is a reasonably accurate proxy for overall intelligence.


This essay is a project of Rethink Priorities. It was written by Jason Schukraft with contributions from Max Carpendale. Thanks to Kim Cuddington, Marcus A. Davis, Peter Hurford, and Daniela Waldhorn for helpful feedback. If you like our work, please consider subscribing to our newsletter. You can see all our work to date here.


  1. Vertebrates constitute a subphylum in the phylum Chordata. Cladistically, it would be more precise to speak of ‘chordates’ and ‘non-chordates.’ In using the terms ‘vertebrates’ and ‘invertebrates’ we defer to common usage. However, the number of invertebrates in the phylum Chordata is trivial compared to the number of invertebrates outside Chordata, so common usage is not wholly inaccurate. ↩︎

  2. We use the terms ‘sentience,’ ‘phenomenal consciousness,’ and ‘subjective experience’ interchangeably. An organism is sentient just in case there is something it is like to be that organism. ‘Valenced experience’ denotes a proper subset of conscious experience in which experiences take on a positive or negative affect. All creatures with the capacity for valenced experience are necessarily sentient, but not all sentient creatures necessarily have the capacity for valenced experience. Note: ‘sentience’ gets used in different ways by different philosophical communities. In philosophy of mind, the term is normally used in its broad sense, to mean ‘phenomenal consciousness.’ (See, inter alia, this SEP article on animal consciousness.) In moral philosophy, the term is normally used in its narrow sense, to mean ‘valenced experience.’ (See, inter alia, this SEP article on the grounds of moral status.) We have adopted the philosophy of mind usage. ↩︎

  3. Colin Allen, James W. Grau, and Mary W. Meagher. 2009. “The Lower Bounds of Cognition: What Do Spinal Cords Reveal?” In J. Bickle (ed.), The Oxford Handbook of Philosophy of Neuroscience (pp. 129–142). Oxford: Oxford University Press. ↩︎

  4. Robert E. Clark and Larry R. Squire. 1998. “Classical Conditioning and Brain Systems: The Role of AwarenessScience 280 (5360): 77–81. ↩︎

  5. W. N. Frost and E. V. Megalou. 2009. “Learning and Memory in Invertebrate Models: Tritonia.” Encyclopedia of Neuroscience, Academic Press: 401-404. ↩︎

  6. Harold M. Pinsker, Wayne A. Hening, Thomas J. Carew, and Eric R. Kandel. 1973. “Long-Term Sensitization of a Defensive Withdrawal Reflex in Aplysia.” Science 07 Dec 1973: Vol. 182, Issue 4116: 1039-1042. Kandel won a Nobel Prize in 2000 for subsequent work on this topic. ↩︎

  7. Humans often experience a similar phenomenon at the dentist. Near the end of a particularly invasive and painful dental procedure, patients will reflexively withdraw from even light contact to the gums, contact that would not have evoked a withdrawal reflex at the beginning of the procedure. ↩︎

  8. Koutarou D. Kimura, Kosuke Fujita and Isao Katsura. 2010. “Enhancement of Odor Avoidance Regulated by Dopamine Signaling in Caenorhabditis elegans.” Journal of Neuroscience 30 (48): 16365-16375. ↩︎

  9. E.M.Eisenstein, D.G.Brunder, and H.J.Blair. 1982. “Habituation and sensitization in an aneural cell: Some comparative and theoretical considerations.” Neuroscience & Biobehavioral Reviews 6: 183-194. ↩︎

  10. Catharine H. Rankin, Thomas Abrams, Robert J. Barry, Seema Bhatnagar, David F. Clayton, John Colombo, Gianluca Coppola et al. 2009. “Habituation revisited: an updated and revised description of the behavioral characteristics of habituation.” Neurobiology of learning and memory 92, no. 2 : 135-138. ↩︎

  11. Monica Gagliano, Michael Renton, Martial Depczynski, Stefano Mancuso. 2014. "Experience teaches plants to learn faster and forget slower in environments where it matters"Oecologia. 175 (1): 63–72. ↩︎

  12. D.C. Wood. 1988. “Habituation in Stentor produced by mechanoreceptor channel modification.” Journal of Neuroscience. 8 (7): 2254–2258. ↩︎

  13. Ronald A. Cohen, Yvonne A. Sparling-Cohen, and Brian Francis O'Donnell. The Neuropsychology of Attention. New York: Plenum Press, 1993. See p. 703. ↩︎

  14. Clint J. Perry, Andrew B Barron, and Ken Cheng. 2013. “Invertebrate Learning and Cognition: Relating Phenomena to Neural Substrate.” Wiley Interdisciplinary Reviews: Cognitive Science 4: 561–82: 566. ↩︎

  15. Theo Mota, Martin Giurfa, and Jean-Christophe Sandoz. 2011. “Color Modulates Olfactory Learning in Honeybees by an Occasion-Setting Mechanism.” Learning and Memory 18: 144-155. ↩︎

  16. Paula Droege. 2017. “The Lives of Others: Pain in Non-Human Animals,” in Jennifer Corns (ed.) The Routledge Handbook of Philosophy of Pain: 196. She adds, “distinguishing flexible from fixed response is not a simple matter. The basic idea behind flexibility is that an animal no longer simply acts based on past associations; it generalizes on past learning to anticipate which sort of action is best” (ibid.). ↩︎

  17. Bennett G. Galef and Kevin N. Laland. 2005. “Social Learning in Animals: Empirical Studies and Theoretical Models.” BioScience 55: 489-499. ↩︎

  18. Sylvain Alem et al. 2016. “Associative Mechanisms Allow for Social Learning and Cultural Transmission of String Pulling in an Insect.” PLOS Biology 14(12): e1002589. ↩︎

  19. See Crickette Sanz, Josep Call, and David Morgan. 2009. “Design complexity in termite-fishing tools of chimpanzees (Pan troglodytes).” Biology Letters 5, no. 3: 293-296 and Nicolas Claidière and Dan Sperber. 2009. “Imitation explains the propagation, not the stability of animal culture.” Proceedings of the Royal Society B: Biological Sciences 277, no. 1681: 651-659. ↩︎

  20. R.W. Byrne. 2003. “Imitation as Behaviour Parsing.” Philosophical Transactions of the Royal Society (B) ↩︎

  21. In rats, nausea seems to play the role of motivating them to engage in pica, the deliberate ingestion of nonfood substances to neutralize toxins. Linda A. Parker. 2003. “Taste avoidance and taste aversion: Evidence for two different processes.” Animal Learning and Behavior 31: 165-172. ↩︎

  22. Parker 2003 ↩︎

  23. Judith R. Ganchrow, Jacob E. Steiner, and Atida Bartana. 1990. “Behavioral reactions to gustatory stimuli in young chicks (Gallus gallus domesticus).” Developmental Psychobiology 23: 103-117. ↩︎

  24. Anne-Sophie Darmaillacq, Ludovic Dickel, Marie-Paule Chichery, Véronique Agin, and Raymond Chichery. 2004. “Rapid taste aversion learning in adult cuttlefish, Sepia officinalis.” Animal Behaviour 68 ( )6: 1291-1298. ↩︎

  25. Parker 2003 ↩︎

  26. Konstantin G Iliadi. 2009. “The Genetic Basis of Emotional Behavior: Has the Time Come for a Drosophila Model?Journal of Neurogenetics 7063. ↩︎

  27. Marc J. Klowden. 2007. Physiological Systems in Insects. London: Academic Press. ↩︎

  28. We use the phrase “pain relief learning” only because it is the accepted nomenclature in the literature. The term is meant to be used in a strictly neutral sense. Read literally, any organism capable of relief from pain is also capable of pain, and thus satisfying this condition would directly entail the capacity for valenced experience. Obviously, we don’t intend to use the term in that way. ↩︎

  29. Gerber, B., A. Yarali, S. Diegelmann, C. T. Wotjak, P. Pauli, and M. Fendt. 2014. “Pain-Relief Learning in Flies, Rats, and Man: Basic Research and Applied Perspectives.” Learning & Memory 21: 232–52. ↩︎

  30. Hiromu Tanimoto, Martin Heisenberg & Bertram Gerber. 2004. “Event Timing Turns Punishment to Reward.” Nature 430: 983. ↩︎

  31. Lynne U. Sneddon et al. 2014. “Defining and Assessing Animal Pain.” Animal Behaviour 97: 202. ↩︎

  32. Reto Bisaz, Alessio Travaglia, and Cristina M. Alberini. 2014. “The neurobiological bases of memory formation: from physiological conditions to psychopathology.” Psychopathology 47, no. 6: 347-356. ↩︎

  33. Sneddon et al. 2014: 202. ↩︎

  34. Ewan St. John Smith and Gary R. Lewin. 2009. “Nociceptors: A Phylogenetic View.” Journal of Comparative Physiology A 195: 1092. ↩︎

  35. Toshiyuki Nakagaki, Ryo Kobayashi, Yasumasa Nishiura, and Tetsuo Ueda. 2004. “Obtaining multiple separate food sources: behavioural intelligence in the Physarum plasmodium.” Proceedings of the Royal Society of London. Series B: Biological Sciences 271, no. 1554: 2305-2310. ↩︎

  36. Voemir Kunchev, Lakhmi Jain, Vladimir Ivancevic, and Anthony Finn. 2006. “Path planning and obstacle avoidance for autonomous mobile robots: A review.” In Gabrys B., Howlett R.J., Jain L.C. (eds) Knowledge-Based and Intelligent Information and Engineering Systems. Springer, Berlin, Heidelberg: 537-544. ↩︎

  37. Andrew B. Barron and Colin Klein. 2016. “What Insects Can Tell Us about the Origins of Consciousness.” Proceedings of the National Academy of Sciences of the United States of America 113 (18): 4900-4908. ↩︎

  38. Shreeya Popat and William Winslade. 2015. “While you were sleepwalking: science and neurobiology of sleep disorders & the enigma of legal responsibility of violence during parasomnia.” Neuroethics 8, no. 2: 203-214. ↩︎

  39. Toshiyuki Nakagaki, Hiroyasu Yamada, and Ágota Tóth. 2000. “Maze-Solving by an Amoeboid Organism.” Nature 407: 470. ↩︎

  40. S.D. Healy and C. Jozet-Alves. 2010. “Spatial Memory.” Encyclopedia of Animal Behavior 304-307. ↩︎

  41. See Table 1 in William Fagan et al. 2013. “Spatial Memory and Animal Movement.” Ecology Letters 16: 1325-1338. ↩︎

  42. Jennifer Mather. 2008. “Cephalopod Consciousness: Behavioural Evidence.” Consciousness and Cognition 17: 37-48. ↩︎

  43. Michael Trestman. 2013. “The Cambrian Explosion and the Origins of Embodied Cognition.” Biological Theory 8: 80-92. ↩︎

  44. Duncan E. Jackson, Stephen J. Martin, Mike Holcombe, and Francis LW Ratnieks. 2006. “Longevity and detection of persistent foraging trails in Pharaoh's ants, Monomorium pharaonis (L.).” Animal Behaviour 71, no. 2: 351-359. ↩︎

  45. Chris R. Reid, Tanya Latty, Audrey Dussutour, and Madeleine Beekman. 2012. “Slime mold uses an externalized spatial “memory” to navigate in complex environments.” Proceedings of the National Academy of Sciences 109, no. 43: 17490-17494. ↩︎

  46. Thus, detour behavior may require an organism to possess the concept object permanence. ↩︎

  47. M.S. Tarsitano and Robert R. Jackson. 1994. “Jumping spiders make predatory detours requiring movement away from prey.” Behaviour 131, no. 1-2: 65-73. ↩︎

  48. Rudiger Wehner. 2003. “Desert ant navigation: how miniature brains solve complex tasks.” Journal of Comparative Physiology A 189, no. 8: 579-588. ↩︎

  49. M.J. Wells. 1964. “Detour Experiments with Octopuses.” Journal of Experimental Biology 41: 621-642. ↩︎

  50. Peter Carruthers. 2007. “Invertebrate Minds: A Challenge for Ethical Theory.” The Journal of Ethics 11: 275-297. It should be noted that Carruthers does not believe that spiders and bees (or any other invertebrates) are moral patients. ↩︎

  51. Paul Willner, Richard Muscat, and Mariusz Pap. 1992. “Chronic Mild Stress-Induced Anhedonia: A Realistic Animal Model of Depression.” Neuroscience and Biobehavioral Reviews 16.4: 525–34 . ↩︎

  52. Jean-Luc Moreau. 2002. “Simulating the anhedonia symptom of depression in animals.” Dialogues in clinical neuroscience 4, no. 4: 351-360. ↩︎

  53. Ariane-Saskia Ries, Tim Hermanns, Burkhard Poeck, and Roland Strauss. 2017. “Serotonin modulates a depression-like state in Drosophila responsive to lithium treatment.” Nature Communications 8: 15738. ↩︎

  54. Learned helplessness was first described in dogs. The classic study on learned helpless is J. Bruce Overmier and Martin E. Seligman. 1967. “Effects of inescapable shock upon subsequent escape and avoidance responding.” Journal of comparative and physiological psychology 63, no. 1: 28-33. ↩︎

  55. Martin E. Seligman. 1968. “Chronic fear produced by unpredictable electric shock.” Journal of Comparative and Physiological Psychology 66, no. 2: 402-411. ↩︎

  56. E.M.Eisenstein, A.D. Carlson, and J.T. Harris. 1997. “A ganglionic model of ‘learned helplessness’.” Integrative Physiological and Behavioral Science, 32(3): 265-271. ↩︎

  57. See chapter 4 in Michael D. Breed and Janice Moore. 2016. Animal Behavior (Second Edition). Academic Press. ↩︎

  58. Meredith Root-Bernstein. 2010. “Displacement Activities during the Honeybee Transition from Waggle Dance to Foraging.” Animal Behaviour 79 (4) : 935–38. ↩︎

  59. Alfonso Troisi. 2002. “Displacement Activities as a Behavioral Measure of Stress in Nonhuman Primates and Human Subjects.” Stress 5 (1): 47-54. ↩︎

  60. Michael C. Appleby and Joy A. Mench. 2004. Poultry Behavior and Welfare. Cambridge, MA: CABI Publishing: 64-65. ↩︎

  61. Root-Bernstein 2010 ↩︎

  62. E. Sunamura et al. 2009. “Intercontinental Union of Argentine ants: Behavioral Relationships among Introduced Populations in Europe, North America, and Asia.” Insectes Sociaux 56: 143-147. ↩︎

  63. Kevin C.F. Fone and M. Veronica Porkess. 2008. “Behavioural and Neurochemical Effects of Post-Weaning Social Isolation in Rodents—Relevance to Developmental Neuropsychiatric Disorders.” Neuroscience & Biobehavioral Reviews 32: 1087-1102. ↩︎

  64. Luc Mounier et al. 2006. “Mixing at the Beginning of Fattening Moderates Social Buffering in Beef Bulls.” Applied Animal Behaviour Science 96: 185-200. ↩︎

  65. Kenneth J. Sufka and Richard A. Hughes. 1991. “Differential Effects of Handling on Isolation-Induced Vocalizations, Hypoalgesia, and Hyperthermia in Domestic Fowl.” Physiology and Behavior 50: 129-133. ↩︎

  66. M.D. Breed. 1983. “Correlations Between Aggressiveness and Corpora Allata Volume, Social Isolation, Age and Dietary Protein in Worker Honeybees.” Insectes Sociaux 30: 482-495. ↩︎

  67. Raphaël Boulay et al. 1999. “Social isolation in ants: Evidence of its impact on survivorship and behavior in Camponotus fellah (Hymenoptera, Formicidae).Sociobiology 33: 111-124. ↩︎

  68. Mathieu Lihoreau, Loïc Brepson, and Colette Rivault. 2009. “The Weight of the Clan: Even in Insects, Social Isolation Can Induce a Behavioural Syndrome.” Behavioural Processes 82: 81-84. ↩︎

  69. GJ Mason and NR Latham. 2004. “Can’t Stop, Won’t Stop: Is Stereotypy a Reliable Animal Welfare Indicator?Animal Welfare 13, S57-69. ↩︎

  70. See Michael C. Appleby and Joy A. Mench. 2004. Poultry Behavior and Welfare. Cambridge, MA: CABI Publishing, especially pp. 151-152. ↩︎

  71. Robert Huber, Adebobola Imeh-Nathaniel, Thomas I. Nathaniel, Sayali Gore, Udita Datta, Rohan Bhimani, Jules B. Panksepp, Jaak Panksepp, and Moira J. van Staaden. 2018. “Drug-sensitive Reward in Crayfish: Exploring the Neural Basis of Addiction with Automated Learning Paradigms.” Behavioural Processes 152: 47-53. ↩︎

  72. Paul L.R. Andrews, Anne-Sophie Darmaillacq, Ngaire Dennison, Ian G. Gleadall, Penny Hawkins, John B. Messenger, Daniel Osorio, Valerie J. Smith, and Jane A. Smith. 2013. “The identification and management of pain, suffering and distress in cephalopods, including anaesthesia, analgesia and humane killing.” Journal of Experimental Marine Biology and Ecology 447: 46-64. ↩︎

  73. Mason and Latham 2004: 58. ↩︎

  74. Arne Öhman. 2000. "Fear and Anxiety: Evolutionary, Cognitive, and Clinical perspectives.” in M. Lewis & J.M. Haviland-Jones (eds.). Handbook of Emotions. pp. 573–93. New York: The Guilford Press. ↩︎

  75. Catherine Belzung and Pierre Philippot. “Anxiety from a Phylogenetic Perspective: Is there a Qualitative Difference between Human and Animal Anxiety?Neural Plasticity Volume 2007, Article ID 59676, 17 pages ↩︎

  76. Such as elevated heart rate, rapid breathing, increased perspiration, increased motor tension, changes in sleeping patterns, and/or changes in food intake. There are many different types of anxiety (e.g., acute versus chronic) and different types of anxiety produce different symptoms. ↩︎

  77. David J. Anderson and Ralph Adolphs. 2014. “A Framework for Studying Emotions across Species.” Cell 157: 187-200. ↩︎

  78. Pascal Fossat, Julien Bacqué-Cazenave, Philippe De Deurwaerdère, Jean-Paul Delbecque, and Daniel Cattaert. 2014. “Anxiety-Like Behavior in Crayfish Is Controlled by Serotonin.” Science 344: 1293-1297. ↩︎

  79. Melissa Bateson et al. 2011. “Agitated Honeybees Exhibit Pessimistic Cognitive Biases.” Current Biology 21: 1070-1073. ↩︎

  80. William T. Gibson et al. 2015. “Behavioral Responses to a Repetitive Visual Threat Stimulus Express a Persistent State of Defensive Arousal in Drosophila.” Current Biology 25: 1401. ↩︎

  81. ibid. The authors add that “such emotion primitives may include the following features or dimensions: persistence following stimulus cessation, scalability (a graded nature of the response), valence, generalization to different contexts, and stimulus degeneracy (different stimuli can evoke the same behavior by induction of a common emotion state).” According to the authors, many of these emotion primitives have been identified in fruit flies. ↩︎

  82. Gordon M. Burghardt. 2011. “Defining and Recognizing Play.” in Nathan and Pellegrini (eds.) The Oxford Handbook of the Development of Play. Oxford University Press. ↩︎

  83. Andreas Berghänel, Oliver Schülke, and Julia Ostner. 2015. “Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off.” Science Advances 1, no. 7: e1500451. ↩︎

  84. Full body tickling induces the same sort of chirping. Marek Spinka , Ruth C. Newberry, and Marc Bekoff. 2001. “Mammalian play: training for the unexpected.” The Quarterly review of biology 76, no. 2: 141-168. ↩︎

  85. Michel Cabanac, Arnaud J. Cabanac, and André Parent. 2009. “The emergence of consciousness in phylogeny.” Behavioural Brain Research 198, no. 2: 267-272. ↩︎

  86. Andrew N. Iwaniuk, John E. Nelson, and Sergio M. Pellis. 2001. “Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.” Journal of Comparative Psychology 115, no. 1: 29-41. ↩︎

  87. Michael J. Kuba, Ruth A. Byrne, Daniela V. Meisel, and Jennifer A. Mather. “When do octopuses play? Effects of repeated testing, object type, age, and food deprivation on object play in Octopus vulgaris.” Journal of Comparative Psychology 120, no. 3: 184-190. ↩︎

Sorted by Click to highlight new comments since:

Ok, finally got around to writing about navigation. A few comments I have about this:
-I agree that navigating known paths/areas is a fairly simple skill. However, if the animal increases the speed with which it traverses such areas it is usually taken as an indicator of becoming familiar with the route. If an animal always moves at a constant speed in a known environment, it may be an indicator that it is constantly in exploring without ever learning.

-The examples presented for navigating unknown areas in the Sentience Table are a bit less clear for me in terms of whether they reflect navigational learning or contextual conditioning. Mazes (as they are generally presented to humans) do seem a reasonable indicator of learning to navigate an unknown area, however, the way they are often used in insect studies means that they primarily test conditioning rather than navigational ability. For instance, the methods used to teach bees to navigate a maze in Zhang et al 2000, were:

Bees were trained to come to a feeder placed initially just outside the entrance to the maze. After they were marked, the feeder was moved slowly step by step through the maze, remaining for ∼1 h in each decision chamber.

As such, it seems to more of an indicator they learnt a series of choices they had to take quite slowly. Likewise, Zhang et al 1996 show bees learning symbolic cues to solve mazes (such as turn right if the wall is green) seem to be more of an indicator of rule learning.
The Drosophila heat aversion paradigm developed by Ofstad et al is quite similar to the Morris water maze, and although this paradigm is a good test of visual-spatial memory (when the animal then quickly changes its position to the new cool point based on movement in the visual panorama), reaching the safe point should be solvable by a Type 1 Braitenberg vehicle (which does not seem to be intelligent).
The examples of maze learning in cockroaches are perhaps a bit more like what humans generally associate with maze learning - I looked back through the references from Webb and Wystrach 2016 and found the original paper on maze learning in cockroaches, where roaches navigated an actual hot metal maze to find a cooler safe point, and it seems their speed and accuracy increased over time.
Perhaps an issue is that maze learning is difficult to motivate insects to do in the same way that vertebrates do. For instance, I think it would be very hard to train a bee to enter a maze and search it for food - placing it (or the entire hive) at the centre seeing if they navigate out might be a better analogy (but I suspect this may just end up with them getting stuck in the corners). That said, I think it is fairly clear that central place foragers navigate unfamiliar territories, it's just that I don't find most uses of mazes to be particularly relevant. The fact that a honeybee hive can be moved to a forest and the bees will quickly forage on available flowers seems a good indication of their ability to navigate unknown areas, but I don't know of anybody who has really tried to quantify this, it's just taken as a given.

-When discussing spatial memory, it's important to consider the distinction of traversing routes vs. having a map like memory. Traversing route (or things like traplining) implies that a set path can be learnt (indicated by landmarks or odometry) but not necessarily that different paths can be linked. However, map memory is taken to imply that routes are placed on a topographic representation in its memory and that an animal can then use this map to link points on known routes with a novel shortcut (that isn’t based on shared landmarks visible between the routes). This is quite controversial and hard to motivate insects to do reliably (as bees and ants tend to try to go to and from their nest on specific routes, but don’t usually jump between routes). I would place this higher than detouring in terms of navigational ability. Actually, I was surprised to see detouring as a navigational ability as I’d never thought about it much. However, I agree that ant work indicates detouring shows a degree of navigational flexibility between direct route following and map navigation. Unfortunately it's probably quite hard to test detouring reliably in flying insects without building large 3D constructs, although some virtual reality work may have done this.

I've enjoyed looking through the criteria and evidence you've used in putting together the Invertebrate Sentinance Table, particularly in that its led me to think place my knowledge of invertebrate neuroscience in a consciousness framework. Feel free to get in touch if you'd like my opinion on any of your further work on this.

Hey Gavin. Once again, thanks for the wealth of insights and references! I have a few thoughts in response, but at this point it might be more valuable if we scheduled a videochat. I'm going to send you a message in a few minutes.

Great post Jason! I have a good background in insect conditioning and navigation from my PhD so I hope that I can provide a useful contribution here.

I would have previously placed a higher weighting on classical conditioning as an indicator for valenced experience, but I wasn't aware of the spinal cord conditioning studies on rodents. The spinal cord is classed as part of the central nervous system so we shouldn't really surprised that it has some capacity for learning. Brains evolved simpler nervous structures which would also have benefited from some learning capability (so I'd expect some learning capacity in jellyfish nerve nets although I'm not sure they've been tested) so it makes sense that peripheral nervous circuits have maintained some capacity for learning, and this is probably evolutionary advantageous as it doesn't put extra cognitive load on the brain.

A headless insect might even have quite a high relative learning capacity compared to a headless rodent (relative in the sense of what can be learnt by the body compared to the intact animal) - the ventral nerve cord (VNC) is quite complex, large relative to the brain (I don't know the neuron ratio between VNC/spinal cord and brain for either vertebrates or insects, could be interesting to find this out), and contains the central pattern generator that coordinates locomotion. I've dissected quite a few insect heads and seen a lot of the bodies get up and walk away while headless. Diptera (flies) can fly while headless as the halteres provide gyroscopic feedback that stabilizes their attitude - once one of my headless hoverflies surprised my colleague when it flew into her hair while she was dissecting moth brains on the other side of the laboratory (true story). So it might be worth checking for studies in insect locomotory conditioning looking at the role of the VNC to see what is possible.

Aside, it's fairly well known that if you do a bad job of cutting the head of a chicken and leave its brain stem intact then it can live quite a long life if it's fed carefully. Would headless chickens fed through straws in a matrix-like factory farm suffer? That fact this feels repulsive while also seeming ethically preferable to factory farming intact chickens means something is wrong with this line of reasoning, right?

Anyway, back to conditioning. Allen et al. 2009 states:

spinal neurons belonging to the nociceptive system are sensitive to both Pavlovian and instrumental relations, and they exhibit a number of phenomena that when studied in normal, intact organisms, including human beings, are frequently described in cognitive or attentional terms. These phenomena include a distractor effect, latent inhibition and overshadowing, and learned helplessness effects.
We have indicated ways we think spinal mechanisms are much more restricted in their capacities than brain mechanisms.

I didn't read the paper in sufficient detail to determine which conditioning phenomena were not present in spinal cords but were possible with intact brains, but I would suggest that those would be better indicators of complex learning that implies valenced experience (likewise, pick the conditioning phenomena that don't occur for sleeping people sleep). For instance, the discrimination can be made between elemental learning (where a stimulus is always reinforced, e.g. A+ B-) and non-elemental learning (where stimuli are not always reinforced, e.g. A+, B+, AB-); the latter is usually taken to imply higher cognitive demands and I would assume that non-elemental learning paradigms cannot be learnt without the intact brain. There are still more complicated associative conditioning tasks like transfer and rule learning that I think would also provide quite a strong indication of complex thought. Honeybees are indeed able to learn all of these in visual and olfactory conditioning tasks (Martin Giurfa has a great review on this, the 2nd section also discusses elemental vs. non-elemental learning and I took the examples from there. Also, see Randolf Menzel (more olfactory) and Mandyam Srinivasan (more visual) for other honeybee learning and memory reviews). Most learning paradigms from honeybees have probably also been tested on Drosophila, but I'm less familiar with that literature.

Likewise with multimodal conditioning that is outside of the usual input-output relationship an organism's experience suggests some cognitive flexibility. For instance, I think the conditioning studies with spinal cords worked on nociceptive reflex circuits that were already present but, I wouldn't expect their spinal cord to learn to associate a smell with a motor action (asides from the fact the neurons from the nose to the spinal cord were cut, imagine you kept all the olfactory neural connections and removed the rest of the rodent brain). However, intact organisms are able to learn to associate say, mechanosensory or visual cues (as a conditioned stimulus) with a food reward (the unconditioned stimulus that induces proboscis extension or salivation), despite the fact that the CS isn't closely linked to a gustatory reflex (whereas smell/taste interacts closely with gustatory circuits).

Ok, I went into a bit more detail on this than planned, but I will come back to operant conditioning and navigation!
Edited a bit for clarity and grammar.

Hi Gavin!

(Apologies for the delayed response; I’ve been traveling the last few days.)

Again, thanks so much for the thoughtful and thought-provoking comments! My background is in philosophy, where the science of these issues gets handled at a rather superficial level, so it’s a pleasure to be able to correspond with someone with such a deep knowledge of the field.

The distinction between operant conditioning and operant conditioning with an unfamiliar action is somewhat arbitrary. We were trying to capture the fact that some types of learning require more cognitive flexibility than others. Perhaps the distinction between elemental and non-elemental learning is a more important one. There are probably a number of other important distinctions that I’ve either glossed over or just missed completely. I think it would be interesting to see a taxonomy of learning abilities and an analysis of which learning abilities give the strongest evidence for valenced experience. I certainly agree with you that contextual learning provides stronger evidence of cognitive flexibility than many other types of learning.

I’m interested to hear more about why you think novelty-seeking behavior might be evidence for the capacity for valenced experience. I suppose the fact that novelty salience can override innate preference is further evidence of behavioral plasticity. Is that what you had in mind or were you thinking of something more specific?

Definitely interested to hear your thoughts about navigation.

Hi Jason, apologies for my delayed reply as well. I’m quite interested in Invertebrate Sentience project and am happy to share some of my knowledge on these topics. My background was originally in robotics and I’ve worked on invertebrate sensory neuroscience from a fairly reductionist viewpoint (and wouldn't previously have been very concerned by questions on consciousness!). While my research was always quite concentrated on vision in flying insects, I felt that I gained quite a well-rounded perspective on invertebrate neuroscience in the labs I worked at and the conference I went to. I think this might be quite common amongst invertebrate neuroscientists - compared to vertebrate fields there are a smaller number of people working on a larger range of organisms so I think there tends to be more intermingling of ideas. Funnily enough, the thing that probably took me longest to adapt to was not treating insects as little input-output automatons but I suspect that if you were to do some insect research your background would lead you to over-anthropomorphise. There is often a fine line between things you can reliably expect insects to do reflexively vs. similar tasks that result in much more variation in what they will do.

Agreed the learning is a complicated issue. My perspective was mostly in trying to separate out things that seem complicated because of the motor component compared to the complexity of the contextual component (which I agree is probably a more important indicator of cognitive flexibility). A taxonomy of learning capability would be interesting (I would assume psychologists have done this for human children), but I wonder if it would necessarily match between taxa - it is possible that different types of phenomenal learning can be performed by a variety of neural architectures, so some organisms may find non-elemental learning easier than elemental learning if that is what they have been exposed to most during evolution.

With regards to novelty, I think it could actually be something quite useful for indicating valanced experience. I’m not an expert on this, but I understand that as well as positively and negatively cued stimulus, novelty can act as a ‘bottom-up’ modulator for selective attention in flies. Further, mutant Drosophila that with abnormal response to novelty are found to have disturbances in learning and memory. Bruno van Swinderen’s lab is doing some interesting work on this, and he has discussed using ‘bottom-up’ modulators to investigate ‘top-down’ selective attention (which seems pretty key to subjective experience in humans). It is possible that novelty is analogous to positive reinforcement in some situations (like developmental learning) but I think Bruno would argue that it can be deeper, because it indicates the animal is actively engaged in learning new information about the world (and I’m sure he’d be happy to talk further on this if you’d like).

I hope to get to replying about navigation tomorrow :)

Ok, I'll discuss operant conditioning a bit here. I may have discounted this a too easily in my comment on part 1 (which was related to sensorimotor control) - I don't think all aspects of operant conditioning necessarily require valanced experience, but it probably does at least require a predictive world model (or efferent copy) which, in itself, seems to be quite cognitively sophisticated.

I've thought a fair bit about operant conditioning in the context of adaptive sensorimotor control that 'fine-tunes' reflexive behaviours (see chapters 3 and 4 of my thesis). I mentioned fixation in my other comment, which is where an insect (say a bee) centers a visual object frontally - the bee has an intrinsically desired world state (object in front) and acts to realize that state, but I do not believe that positioning the object frontally really counts as positive valance for her. However, the bee is able to learn to change how it responds to discrepancies in the desired world state (say the polarity coupling her yaw torque to the world is inverted, she will learn to turn right to make the object turn right, instead of the normal situation of turning left to make an object on her left move rightwards) and one hypothesis is that the bee can make this adaption because it not only has both a desired world state and motor control program it would normally use to achieve that state, but also makes a prediction of how it's actions will affect the world. In the event that the bee observes the results of its actions no longer match its predictions, and before she reverses the polarity of its yaw control, the bee may first update her world model to reflect the fact that it should now expect the world to turn in the opposite direction, from which the new predictions can be used to update the world model. Predictive models are an old idea from psychology that were explored in Drosophila using behavioral experiments before a neural circuit implementing an efferent copy was identified in them. The whole world model thing sounds rather abstract but has some real world examples, such as a growing animal learns that adapts its gait to longer legs, or an insect that adapts its flight muscle output to compensate for wing wear, and it also seems to have a relatively simple neural implementation in Drosophila that doesn't really code for much information about about the world. Of course the appearance of adaptive sensory motor control may not necessarily require a predictive world model, and it is possible that a robust motor control scheme could pre-code responses to enough conditions to appear adaptive, but given that insects have small brains I'd suggest a basic adaptive process is involved. See Section 6.2.4 in my thesis for a more in depth discussion on adaptive control and extra literature references.

I agree that the classic case of operant conditioning (like learning to do something for a reward) does imply valanced experience (I don't think that showing a conditioned reflex like salivating necessarily reduces the strength of this evidence). However, I don't entirely agree with how you are phrasing learning new or unfamiliar actions - it would help to be more specific. In most cases what is being learnt is the use of known actions in new contexts or novel combinations of known actions (in known or novel contexts) - I think that learning a new action is quite rare. Let me elaborate - an adult rat (post development) probably knows how to push things in general (and indeed make most other motor actions its body is capable of) but it needs to form the association that applying the known pushing action to a lever gives it a reward. Likewise, the soccer playing bumblebees knew how to walk and probably more or less knew how to push things, but they had to learn to do this in sequence to get the ball to the reward point. Teach a rat (or bumblebee) to handstand an I will agree you've taught it a new action. Why make this distinction? The cognitive flexibility associated with learning to use known actions in new contexts seems different from learning new motor skills, and what should be assessed be assessed is the novelty of the context in the former case and the novelty of the action in the later case. Learning new combinations of known movements seems somewhere in between contextual and motor learning. Most organisms do motor learning during development when they have an intrinsic motivation to learn how to use their bodies (and the learning probably involves changing spinal cord type circuits), so I'd suggest that contextual learning provides stronger evidence for cognitive flexibility (I don't know if any literature supports this, this is a distinction just became apparent to me when reading this post).

As an aside, I don't think you've mentioned novelty seeking behaviour yet? I was peripherally involved in a study that shows honeybee choose to look a novel stimulus over a recently experienced stimulus in the absence of any specific reward. I'm not really sure how this fits into the framework of this study, but learning could be a good place to consider this.

I hope to get to navigation in the next of my mini-series of comments..

Edited a bit for clarity and grammar (without breaking the formatting as I did in my other comment).

Play behavior is in general not found in birds, with the exception of the highly intelligent corvid family


You forgot kea and cockatoo parrots. https://www.abc.net.au/news/2020-12-26/birds-that-play-are-smarter-finds-gisela-kaplan-research/12990902

Also, possibly emu (https://www.buzzfeed.com/annamenta/you-go-emu-you-play-fetch), which have among the largest brains in the bird world.

Curated and popular this week
Relevant opportunities