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Authors: John Bradshaw

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The complexity of these relationships seems to have arisen as the mammalian emotional repertoire evolved piecemeal from that of ancient reptiles, which have much simpler emotional lives (or even, some scientists argue, none at all). Likewise, each emotion is not located in its own unique part of the mammalian brain. Rather, most emotions appear to arise in parts of the midbrain, which is connected to the spinal cord through the hindbrain and, in mammals, is almost completely encased inside the much larger forebrain, the “thinking” part of the brain. Two structures in the midbrain that are key to the generation of many emotions are the hypothalamus and the amygdalae, but these structures are also engaged in other functions, such as hunger, thirst, the sleep-wake cycle, and learning.

Despite this complexity, it is clear that emotions have a physical presence in the brain and that they are associated with changes in hormones circulated around the body; in short, they have predictable physical manifestations. Thus a combination of the two aforementioned approaches—the physiological (Emotion I) and the behavioral (Emotion II) can be used to investigate which emotions dogs almost certainly possess and which they almost certainly don't.

Emotions can be placed in a rough hierarchy from the most primitive (i.e., those that are thought to have appeared first in the evolution of the vertebrates) to the most complex. Since dogs are mammals like us but have less complex brains than our own, it is logical to conclude that
we share the simpler emotions but also that the most complex emotions experienced by humans are likely to be ours alone.

The most basic emotions—such as hunger, thirst, pain, and sexual desire—are perhaps better described as “feelings” than as “emotions.” They are primarily processed by the most primitive parts of the brain—the brainstem, the midbrain, and the hypothalamus. The hypothalamus also processes information relating to reward and punishment; it is therefore crucial to the way that dogs learn.

The simplest of the true emotions—fear, anger, anxiety, and happiness—are often referred to as “primes.” These are “instinctive” in that they do not have to be learned: No one has to learn how to be frightened; it just happens. They are also “basic” in the sense that they are generated by the most primitive part of the mammalian brain, the limbic system, which appeared very early in the evolution of the vertebrates, perhaps as far back as 500 million years ago. It is therefore almost inconceivable that dogs should not possess these emotions, although it is difficult to gauge precisely what their subjective experience is like.

Fear, anger, anxiety, and happiness all evolved as ways of responding to significant threats or opportunities. One way of looking at them is to see them as providing “shortcuts.” For example, an animal doesn't have to scan its memory for the specific threat it is encountering at a particular time and then devise a response; rather, it is prompted by its emotional reaction (fear) to run away quickly, after which it can determine from a safe distance what the threat actually was. This is not to say that learning doesn't play a part in categorizing such threats more accurately based on accumulated experiences; nevertheless, the underlying emotion will almost always stay the same from one such experience to another.

Fear
may be the most primitive emotion of them all. As for the other simple emotions, the amygdalae, paired almond-shaped structures buried deep in the center of the brain, play a central role in both forming and retrieving memories of frightening events and also in generating the response. The posterior part of the hypothalamus is another key structure, relaying information to and from the brain and out to other hormone-producing structures, such as the adrenal glands that produce the fight-or-flight hormone adrenaline.

The expression of fear in dogs follows a pattern that is recognizably similar to the expression of fear in man. It usually begins with the dog becoming suddenly alert and then freezing, rooted to the spot while the amygdalae furiously signal to the cortex, the “thinking” part of the brain, for the correct response to the situation. Meanwhile, the dog holds itself tensely, possibly shaking visibly, with eyes wide and teeth bared, as a general preparation for all things dangerous. Beneath the skin, the heart rate and breathing both speed up.

If the situation is unprecedented, there may be nothing helpful in the memory databank. This can lead to behavior that may seem downright bizarre to us more logical humans. For example, a dog that has never seen a cardboard box before in its life may fail to identify it as a harmless inanimate object and, by default, go into a full-blown fear response.
8
Fear is a shortcut for categorizing events, and what falls into the “scary” category depends upon what the dog has experienced before, and what it hasn't, especially during the first six months of its life. The “scary” category will consist of two sorts of things: those that have frightened the dog in the past, and those the dog has had no experience of whatsoever.

The dog's response to the scary situation will depend on what it has found to work best in the past. Some dogs will almost always freeze; others will usually run away. Still others, especially if their escape route has been blocked on previous occasions, may resort to aggression almost immediately. Indeed, many clinicians will tell you that most of the cases of aggression they see are motivated by fear—not by anger, or any need to “dominate.” Fear also lies at the heart of many other behavioral disorders. It is arguably the most powerful of the emotions that dogs possess.

Fear is a powerful trigger of learning. Dogs that are suddenly frightened by something unfamiliar, such as a cardboard box, are likely not only to continue to be frightened by similar boxes but may also show palpable signs of apprehension when they revisit the place where the original fright occurred, even though the scary object is no longer there. This is one way that dogs can develop what appear to us to be “irrational” fears—although they presumably make perfect sense to the
dog, who is recalling the whole event, not just the “obvious” unfamiliar stimulus.

Anxiety
is sometimes confused with fear, in that it shares some of the same manifestations. But anxiety is about the
anticipation
of fear—it is triggered not by an actual object or event that is intrinsically frightening but, rather, by predictors of a frightening event that may occur at some indeterminate time in the future. My first two dogs, Alexis and Ivan, both Labrador/terrier crosses (Jack Russell and Airedale respectively), were self-confident to the extent that I doubt they ever felt much anxiety. My third, Bruno, was a purebred Labrador, and an altogether more emotionally dependent animal—not easily frightened but very reliant on the humans around him. Before he arrived at our house as an eight-week old puppy nearly thirty years ago, I had never heard of “separation anxiety”—nor had many veterinarians, ours included. Fifteen years later, I started a research program that revealed, among other things, that half the young Labradors in the UK hate being left alone; but in those days I don't think anyone even suspected that this was the case.

Bruno could not hide the anxiety he felt whenever he realized that we were about to go out. Locating car keys, putting on coats, collecting children from the four corners of the house—these actions triggered an expression of absolute misery on his face, and he slunk off to his bed, the place he felt most secure. The “experts” at the time told us that this was only a game he was playing to stop us going out, that gundogs were bred to be left in kennels for hours at a time and were perfectly happy doing so. As soon as we were gone, we were told, he would settle down and sleep until we returned. Wrong: His ongoing anxiety was obvious from the chewed-up bed, furniture, even wallpaper that we found when we returned home.

These are all signs of anxiety. Retrievers are very mouth-focused, and chewing seems to be their favorite way of relieving tension; if Bruno had been a different type of dog, he might have barked, paced, scratched at the walls, or urinated or defecated on the floor. When we tried to put him in boarding kennels, where the opportunities for chewing were limited, he turned to howling—for hours at a time. In the end
we accepted that he was just a very attached dog and tried to make sure that he was always with someone he knew. He wasn't
frightened
of our going out, but he knew that he hated being left alone, so the signs that told him that he was about to be left made him anxious. He was probably also anxious that we would never return: Dogs' concept of time is not fully understood but seems less precise than our own, so it is difficult to know how much they can anticipate things that might or might not happen at some indeterminate time in the future.

Anger
is not the same as fear. Both can lead to aggression, which is why the two emotions are often confused. But in fact they are readily distinguishable based on the dog's body-language.

Fear arises when the dog's brain identifies potentially damaging situations that are outside its control; anger occurs when the dog's expectations of the world are threatened. For example, dogs who are very attached to what they perceive as their territory will become angry when another dog (especially one of the same sex) intrudes into that territory. An angry dog, much like a fearful dog, will probably growl and bare its teeth, but these are primarily signals of intent and only secondarily expressions of emotion. It is easy to tell the difference between a fearful dog and an angry dog. The fearful dog will obviously be trying to escape, with everything from its ears to the corners of its mouth pulled backward, and if given the opportunity it will most likely actually run away. The angry dog will be stiffened and poised to move forward to counter the threat.

Anger, like all emotions, is an evolved survival mechanism, but also one that has been radically altered by domestication. A wolf that never defended its food or resting space from other wolves would not live for very long in the wild. However, the capacity to feel and express anger is less of an asset to domestic dogs, whose survival is crucially dependent on their owners' goodwill rather than on competition with others of their own kind. Indeed, domestication has raised the dog's threshold for anger to the point where most dogs rarely become angry.

Dog trainers who still regard dominance as the key motivator for dog behavior tend to explain most aggressive behavior as driven by anger—specifically, anger arising from the dog's perception that its “status” in
the household has been challenged. This notion is almost certainly based upon a misinterpretation of what actually motivates most dogs. However, it would be irresponsible to insist that dogs never become angry, that they never try to assert themselves over other dogs or challenge people who they think are trying to deny them something they value highly. For example, some dogs are highly territorial and will bark when their territory is invaded to show that they are angry at the intrusion. Among wild animals, ignoring such a threat would lead to actual aggression; the combined effects of domestication and training make this much less likely to occur in domestic dogs.

Although dogs are much less reactive than wolves are, they still need to be taught emotional control, so they can coexist peacefully alongside people and other dogs. In the wild, one of the crucial lessons that mothers teach their offspring is to inhibit their bite: Puppies' teeth can't do much damage, but it's essential that they learn to control the amount of force they apply when biting, so that they don't hurt their littermates while playing. Otherwise a full-scale fight could ensue. Moreover, once they have their adult teeth, uninhibited biting can cause serious injury. In the same way that they can learn to control their biting, an expression of anger, dogs can learn to control anger itself. A dog that is never taught the consequences of its expressions of anger has the potential to become at least a nuisance and at worst a danger to society and to itself. Dogs need to be taught boundaries, and by this I mean emotional boundaries even more than physical boundaries; permissiveness, allowing the dog to do as it pleases, is not humane. In nature, such behavior would quickly be met by either aggression or avoidance, neither of which promotes survival in a social species. In human society, dogs cannot afford such trial and error, which ultimately leads to the pound or to euthanasia.

There is a very small minority of dogs that occasionally become aggressive without displaying any signs of fear or anger. It's often unclear whether such dogs are true “psychopaths,” whose emotions are abnormal, or whether they are simply able to inhibit the normal signals that would otherwise disclose their intentions. Such dogs are valued in the small sections of society where dogs are used primarily as weapons, but they are otherwise unsuited to life alongside humanity. This is not to say that all “fighting dogs” are psychopaths; many have been trained
to become instantly aggressive on command, behavior that is potentially reversible.

Such unannounced aggressive tendencies should not be confused with the “aggression” that, in the wolf, is an essential aspect of predatory behavior. A dog that kills a sheep may casually be referred to as “aggressive,” but it is highly unlikely that the dog was frightened of the sheep or perceived it as a rival; rather, it was simply, if unacceptably, obeying the instinct to hunt. Motivationally, predatory “aggression” is quite distinct from aggression driven by anger or fear—for example, it is controlled by a completely different part of the hypothalamus—and if it has an emotional component, this is less likely to be negative than positive. (Predators should be motivated to find hunting “fun,” which would ensure that they keep doing it.)

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