Theory of mind in animals

History and development

The term "theory of mind" was originally proposed by Premack and Woodruff in 1978. Early studies focused almost entirely on studying if chimpanzees could understand the knowledge of humans. This approach turned out not to be particularly fruitful and 20 years later, Heyes, reviewing all the extant data, observed that there had been "no substantial progress" in the subject area.

A 2000 paper approached the issue differently by examining competitive foraging behaviour between primates of the same species (conspecifics). This led to the rather limited conclusion that "chimpanzees know what conspecifics do and do not see". Next, brain activity in higher primates was studied and as a result, a 2003 study of the human brain suggested that the a functioning ToM system activated three major nodes, the medial prefrontal, superior temporal sulcus, and inferior frontal: the medial prefrontal node handles the mental state of the self, that the superior temporal sulcus detects the behaviour of other animals and analyzes the goals and outcomes of this behaviour, and the inferior frontal region maintains representations of actions and goals.

In 2007, Penn and Povinelli wrote "there is still little consensus on whether or not nonhuman animals understand anything about unobservable mental states or even what it would mean for a non-verbal animal to understand the concept of a 'mental state'." They went on further to suggest that ToM was "any cognitive system, whether theory-like or not, that predicts or explains the behaviour of another agent by postulating that unobservable inner states particular to the cognitive perspective of that agent causally modulate that agent's behaviour".

In 2010, an article in Scientific American acknowledged that dogs are considerably better at using social direction cues (e.g. pointing by humans) than are chimpanzees. In the same year, Towner wrote, "the issue may have evolved beyond whether or not there is theory of mind in non-human primates to a more sophisticated appreciation that the concept of mind has many facets and some of these may exist in non-human primates while others may not." Horowitz, working with dogs, agreed with this and suggested that her recent results and previous findings called for the introduction of an intermediate stage of ability, a rudimentary theory of mind, to describe animals' performance.

In 2013, Whiten reviewed the literature and concluded that regarding the question "Are chimpanzees truly mentalists, like we are?", he stated he could not offer an affirmative or negative answer. A similarly equivocal view was stated in 2014 by Brauer, who suggested that many previous experiments on ToM could be explained by the animals possessing other abilities. They went on further to make reference to several authors who suggest it is pointless to ask a "yes or no" question, rather, it makes more sense to ask which psychological states animals understand and to what extent. At the same time, it was suggested that a "minimal theory of mind" may be "what enables those with limited cognitive resources or little conceptual sophistication, such as infants, chimpanzees, scrub-jays and human adults under load, to track others' perceptions, knowledge states and beliefs."

In 2015, Cecilia Heyes, Professor of Psychology at the University of Oxford, wrote about research on ToM, "Since that time [2000], many enthusiasts have become sceptics, empirical methods have become more limited, and it is no longer clear what research on animal mindreading is trying to find" and "However, after some 35 years of research on mindreading in animals, there is still nothing resembling a consensus about whether any animal can ascribe any mental state" (Heyes' emphasis). Heyes further suggested that "In combination with the use of inanimate control stimuli, species that are unlikely to be capable of mindreading, and the 'goggles method' [see below], these approaches could restore both vigour and rigour to research on animal mindreading."

Methods

Specific categories of behaviour are sometimes used as evidence of animal ToM, including imitation, self-recognition, social relationships, deception, role-taking (empathy), perspective-taking, teaching and co-operation, however, this approach has been criticised. Some researchers focus on animals' understanding of intention, gaze, perspective, or knowledge, i.e. what another being has seen. Several experimental methods have been developed which are widely used or suggested as appropriate tests for nonhuman animals possessing ToM. Some studies look at communication between individuals of the same species (intraspecific) whereas others investigate behaviour between individuals of different species (interspecific).

Knower-Guesser

The Knower-Guesser method has been used in many studies relating to animal ToM. Animals are tested in a two-stage procedure. At the beginning of each trial in the first discrimination training stage, an animal is in a room with two humans. One human, designated the "Guesser," leaves the room, and the other, the "Knower," baits one of several containers. The containers are screened so that the animal can see who does the baiting, but not where the food has been placed. After baiting, the Guesser returns to the room, the screen is removed, and each human points directly at a container. The Knower points at the baited container, and the Guesser at one of the other three, chosen at random. The animal is allowed to search one container and to keep the food if it is found.

Competitive feeding paradigm

The competitive feeding paradigm approach is considered by some as evidence that animals have some understanding of the relationship between "seeing" and "knowing".

At the beginning of each trial in the paradigm, a subordinate animal (the individual thought to be doing the mind-reading) and a dominant animal are kept on opposite sides of a test arena which contains two visual barriers. In all trials, a researcher enters the enclosure and places food on the subordinate's side of one of the visual barriers (one baiting event), and in some trials the researcher re-enters the enclosure several seconds later and moves the food to the subordinate's side of the other visual barrier (second baiting event). The door to the subordinate's cage is open during any baiting by the researcher. The conditions vary according to whether the dominant's door is open or closed during the baiting events, and therefore whether the subordinate individual can see the dominant. After baiting, both of the animals are released into the test arena, with the subordinate being released several seconds before the dominant. If the animals possess ToM, it is expected that subordinates are more likely to gain the food, and more likely to approach the food under several circumstances: (1) When the dominant's door is closed during trials with a single baiting event; (2) when the dominant's door is open during a first baiting event but closed during a second; (3) in single baiting event trials with the dominant's door open, subordinates are more likely to get the food when they compete at the end of the trial with a dominant individual who did not see the baiting.

Goggles Method

In one suggested protocol, chimpanzees are given first-hand experience of wearing two mirrored visors. One of the visors is transparent whereas the other is not. The visors themselves are of markedly different colours or shapes. During the subsequent test session, the chimpanzees are given the opportunity to use their species-typical begging behaviour to request food from one of the two humans, one wearing the transparent visor and the other wearing the opaque. If chimpanzees possess ToM, it would be expected they would beg more often from the human wearing the transparent visor.

False Belief Test

A method used to test ToM in human children has been adapted for testing non-human animals. The basis of the test is to track the gaze of the animal. One human hides an object in view of a second human who then leaves the room. The object is then removed. The second human returns whereupon they will mistakenly look for the object where they last saw it. If the animal stares first and longest at the location where the human last saw the object, this suggests they expect him to believe it is still hidden in that place.

In nonhuman primates

Many ToM studies have used nonhuman primates (NHPs). One study that examined the understanding of intention in orangutans (Pongo pygmaeus), chimpanzees (Pan troglodytes) and children showed that all three species understood the difference between accidental and intentional acts.

Chimpanzees

There is controversy over the interpretation of evidence purporting to show ToM in chimpanzees.

William Field and Sue Savage-Rumbaugh have no doubt that bonobos have evolved ToM and cite their communications with a well-known captive bonobo (Pan paniscus), Kanzi, as evidence.

However, empirical studies show that chimpanzees are unable to follow a human's gaze, and are unable to use other human-eye information. Attempts to use the "Goggles Method" (see above) on highly human-enculturated chimpanzees failed to demonstrate they possess ToM.

In contrast, chimpanzees use the gaze of other chimpanzees to gain information about whether food is accessible. Subordinate chimpanzees are able to use the knowledge state of dominant chimpanzees to determine which container has hidden food.

If chimpanzees can see two opaque boards on a table and are expecting to find food, they do not choose a board lying flat because if food was under there, it would not be lying flat. Rather, they choose a slanted board, presumably inferring that food underneath is causing the slant. Chimpanzees appear able to know that other chimpanzees in the same situation make a similar inference. In a foraging game, when their competitor had chosen before them, chimpanzees avoided the slanted board on the assumption that the competitor had already chosen it. In a similar study, chimps were provided with a preference box with two compartments, one containing a picture of food, he other containing a picture of nothing (the pictures had no causal relation to the contents). In a foraging competition game, chimpanzees avoided the chamber with the picture of food when their competitor had chosen one of the chambers before them. The authors suggested this was presumably on the assumption that the competitor shared their own preference for it and had already chosen it.

One study tested another sensory mode of ToM. In a food competition, a human sat inside a booth with one piece of food to their left and one to their right. The food could be withdrawn from the competing chimpanzee's reach when necessary. In the first experiment, the chimpanzee could approach either side of the booth unseen by the human, but then had to reach through either a transparent or opaque tube to get the food. In a second experiment, both were transparent and the human was looking away, but one of the tubes made a loud rattle when it was opened. Chimpanzees reached through the opaque tube in the first experiment and the silent tube in the second. The chimpanzees successfully concealed their food-stealing from their human competitor in both cases.

Chimpanzees have passed the False Belief Test (see above) involving anticipating the gaze of humans when objects have been removed.

Other primates

In one approach testing monkeys, rhesus macaques (Macaca mulatta) are able to "steal" a contested grape from one of two human competitors. In six experiments, the macaques selectively stole the grape from a human who was incapable of seeing the grape, rather than from the human who was visually aware. The authors suggest that rhesus macaques possess an essential component of ToM: the ability to deduce what others perceive on the basis of where they are looking. Similarly, free ranging rhesus macaques preferentially choose to steal food items from locations where they can be less easily observed by humans, or where they will make less noise.

A comparative psychology approach tested six species of captive NHPs (three species of great apes: orangutans, gorillas, chimpanzees, and three species of old-world monkeys: lion-tailed macaques (Macaca silenus), rhesus macaques and collared mangabeys (Cercocebus torquatus)) in a "hide and seek" game in which the NHPs played against a human opponent. In each trial, the NHP has to infer where food has been hidden (either in their right or left hand) by the human opponent. In general, the NHPs failed the test (whereas humans did not), but surprisingly, performances between the NHP species did not reveal any inter-species differences. The authors also reported that at least one individual of each of the species showed (weak) evidence of ToM.

In a multi-species study, it was shown that chimpanzees, bonobos and orangutans passed the False Belief Test (see above).

In 2009, a summary of the ToM research, particularly emphasising an extensive comparison of humans, chimpanzees and orang-utans, concluded that great apes do not exhibit understanding of human referential intentions expressed in communicative gestures, such as pointing.

Parrots

African grey parrots (Psittacus erithacus) have demonstrated high levels of intelligence. Irene Pepperberg did experiments with these and her most accomplished parrot, Alex, demonstrated behaviour which seemed to manipulate the trainer, possibly indicating theory of mind.

Ravens

Ravens are members of the corvidae family and are widely regarded as having complex cognitive abilities.

Food-storing ravens cache (hoard) their food and pilfer (steal) from other ravens' caches. They protect their caches from being pilfered by conspecifics using aggression, dominance and re-caching. Potential pilferers rarely approach caches until the storing birds have left the cache vicinity. When storers are experimentally prevented from leaving the vicinity of the cache, pilferers first search at places other than the cache sites. When ravens (Corvus corax) witness a conspecific making caches, to pilfer those caches they (1) delay approaching the cache only when in the presence of the storer, and (2) quickly engage in searching away from the caches when together with dominant storers. These behaviours raise the possibility that ravens are capable of withholding their intentions, and also providing false information to avoid provoking the storer's aggression to protect its cache. Ravens adjust their pilfering behaviour according to when the storers are likely to defend the caches. This supports the suggestion that they are deceptively manipulating the other's behaviour. Other studies indicate that ravens recall whom was watching them during caching, but also know the effects of visual barriers on what competitors can and can not see, and how this affects their pilfering.

Ravens have been tested for their understanding of "seeing" as a mental state in other ravens. It appears they take into account the visual access of other ravens, even when they cannot see the other raven.

In one study, ravens were tested in two rooms separated by a wooden wall. The wall had two functional windows that could be closed with covers; each cover had a peephole drilled into it. In the next familiarization step, the ravens are trained to use a peephole to observe and pilfer human-made caches in the adjacent room. Under test conditions, there was no other raven present in the adjacent room, however, a hidden loudspeaker played a series of sounds recorded from a competitor raven. The storing raven generalized from their own experience when using the peephole to pilfer the human-made caches and predicted that the audible (raven) competitors could potentially see their caches through the peep-hole and took appropriate action, i.e. the storing ravens finished their caches more quickly and they returned to improve their caches less often. The researchers pointed out that this represented "seeing" in a way that cannot be reduced to the tracking of gaze cues – a criticism leveled at many other studies of ToM. The researchers further suggested that their findings could be considered in terms of the "minimal" (as opposed to "full-blown") ToM recently suggested.

Using the Knower-Guesser approach, ravens observing a human hiding food are capable of predicting the behaviour of bystander ravens that had been visible at both, none or just one of two baiting events. The visual field of the competitors was manipulated independently of the view of the test-raven. The findings indicate that ravens not only remember whom they have seen at caching but they also take into account that the other raven's view was blocked.

Scrub jays

Scrub jays are also corvids. Western scrub jays (Aphelocoma californica) both cache food and pilfer other scrub jays' caches. They use a range of tactics to minimise the possibility that their own caches will be pilfered. One of these tactics is to remember which individual scrub jay watched them during particular caching events and adjust their re-caching behaviour accordingly. One study with particularly interesting results found that only scrub jays which had themselves pilfered would re-cache when they had been observed making the initial cache. This has been interpreted as the re-caching bird projecting its own experiences of pilfering intent onto those of another potential pilferer, and taking appropriate action. Another tactic used by scrub jays is if they are observed caching, they re-cache their food when they are subsequently in private. In a computer modeling study using "virtual birds", it was suggested that re-caching is not motivated by a deliberate effort to protect specific caches from pilfering, but by a general motivation to simply cache more. This motivation is brought on by stress, which is affected by the presence and dominance of onlookers, and by unsuccessful recovery attempts.

In dogs

Domestic dogs (Canis familiaris) show an impressive ability to use the behaviour of humans to find food and toys using behaviours such as pointing and gazing. The performance of dogs in these studies is superior to that of NHPs, however, some have stated categorically that dogs do not possess a human-like ToM.

The Guesser-Knower approach has been used with ToM studies in dogs. In one study, each of two toys was placed on the dog's side of two barriers, one opaque and one transparent. In experimental conditions, a human sat on the opposite side of the barriers, such that they could see only the toy behind the transparent barrier. The human then told the dog to 'Fetch' without indicating either toy in any way. In a control, the human sat on the opposite side but with their back turned so that they could see neither toy. In a second control, the human sat on the same side as the dog such that they could see both toys. When the toys were differentiable, dogs approached the toy behind the transparent barrier in experimental as compared to "back-turned" and "same-side" condition. Dogs did not differentiate between the two control conditions. The authors suggested that, even in the absence of overt behavioural cues, dogs are sensitive to others' visual access, even if that differs from their own. Similarly, dogs preferentially use the behaviour of the human Knower to indicate the location of food. This is unrelated to the sex or age of the dog. In another study, 14 of 15 dogs preferred the location indicated by the Knower on the first trial, whereas chimpanzees require approximately 100 trials to reliably exhibit the preference.

Human infants (10 months old) continue to search for hidden objects at their initial hiding place, even after observing them being hidden at another location. This perseverance of searching errors is at least partly contributed to by behavioural cues from the experimenter. Domestic dogs also commit more search errors in communicative trials than in non-communicative or non-social hiding trials. However, human-encultured wolves (Canis lupus) do not show this context-dependent perseverance in searching. This common sensitivity to human communication behaviour may arise from convergent evolution.

Dogs which have been forbidden to take food are more likely to steal the food if a human observer has their back turned or eyes closed than when the human is looking at them. Dogs are also more likely to beg for food from an observer whose eyes are visible compared to an observer whose eyes are covered by a blindfold.

In a study of the way that dogs interact, play signals were sent almost exclusively to forward-facing partners. In contrast, attention-getting behaviors were used most often when the other dog was facing away, and before signaling an interest to play. Furthermore, the type of attention-getting behaviour matched the inattentiveness of the playmate. Stronger attention-getting behaviours were used when a playmate was looking away or distracted, less forceful ones when the partner was facing forward or laterally,

In pigs

An experiment at the University of Bristol found that one out of ten pigs was possibly able to understand what other pigs can see. That pig observed another pig which had view of a maze in which food was being hidden, and trailed that pig through the maze to the food. The other pigs involved in the experiment did not.

In goats

A 2006 study found that goats exhibited intricate social behaviours indicative of high-level cognitive processes, particularly in competitive situations. The study included an experiment in which a subordinate animal was allowed to choose between food that a dominant animal could also see and food that it could not; those who were subject to aggressive behaviour selected the food that the dominant animal could not see, suggesting that they are able to perceive a threat based on being within the dominant animal's view – in other words, visual perspective taking.