Mood and Emotion
Last revised April 27, 2017.
Mood and Emotion.1
Sy Montgomery writes “hormones and neurotransmitters, the chemicals associated with human desire, fear, love, joy, and sadness, are highly conserved across taxa… This means that whether you’re a person or a monkey, a bird or a turtle, an octopus or a clam, the physiological changes that accompany our deepest-felt emotions (moods) appear to be the same. Even a brainless scallop’s little heart beats faster when the mollusk is approached by a predator, just like yours or mine would do were we to be accosted by a mugger.2”
We often use the words “mood” and “emotion” interchangeably, but there are differences between the two concepts.
- Moods are background states that are less specific than emotions and that have a biological counterpart. Moods differ in valence (positive/negative) and strength (mild/intense), but don’t have any “cognitive” component. They are states that influence how we feel, but don’t direct specific action toward any target. Moods may not be immediately noticed by the one experiencing them. They may last longer than emotions. They may be less intense than emotions. They are usually not triggered by any specific thing or event. Some moods: anxious, calm, contented, depressed, excited, fearful, happy, relaxed, sad.
- Emotions are like moods, but aren’t completely accounted for by biology — they also have a cognitive layer that provides them with a context, an explanation, a rationale. And they have behavioral and subjective components, too.3 Emotions are likely to accompany a mood. Emotions often have an object: When you feel jealousy, you are jealous of someone. When you are annoyed, you are annoyed by something or someone.
I suspect that most animals have moods. Certainly your horse does. The dogs, horses, and humans in our lives all seem to have emotions, too. My horse shows his affection when he licks my hand and arm again and again, or when he rubs his head in my arm pit. Perhaps he shows it when, on the trail, he goes around a branch that is high enough that he can pass under, but low enough that it is in my way. He shows his anger when he pins his ears back or raises a leg when I am brushing him in his stall, and he is trying to eat. He shows his curiosity when he meets me, and sniffs my hands and pockets for signs of carrot. In his early days with me, my mule showed his distrust when he backed up as I entered his stall, or kept just a few feet away from me when I was trying to catch him in the pasture. Both show euphoria when I scratch their necks and chins — by lowering their heads, closing their eyes, relaxing their lower lip. Both show grief when I take one out of the barn, leaving the other behind. They show hope when they try again and again during clicker training. Bud felt panic a few weeks ago when a long lead line wrapped around his legs and he fell down repeatedly. And when my horse reaches a scary bridge that he is afraid to cross, and I dismount and walk across it, he follows me, showing trust. You may find evidence of these emotions — and perhaps others — in your horse.
In this chapter, I explore a horse’s moods and emotions, in part by looking at the connections between them and physiology. Because the physiology of the horse is so much like the physiology of a human, we can connect the mood or emotion of humans to a physiological state, and in the horse we can infer a mood or emotion from that physiological state.
Assessing Mood or Emotion in Humans
Most animals do not have expressive faces like humans and other primates. So we need to read into their behaviors or physiology, and make inferences. Humans claim to have hundreds of emotions. Doubt me? Complete the following statement using all of the emotion words below that you are feeling.4 “Right now I feel…”
Absorbed · Adoration · Affection · Afraid · Aggravated · Alarmed · Alienated · Amazed · Ambivalent · Amused · Angry · Anguished · Annoyed · Anticipating · Anxious · Apathy · Aroused · Attraction · Awe · Awkward · Bitter · Bored · Brave · Calm · Caring · Cautious · Cheerful · Comfortable · Compassionate · Concern · Confident · Confused · Contempt · Content · Courageous · Curious · Defeated · Delighted · Depressed · Desirous · Despairing · Disappointed · Disgraced · Disgusted · Disillusioned · Disliked · Dismayed · Disoriented · Distrusting · Disturbed · Dreading · Eager · Ecstatic · Elated · Embarrassed · Empathic · Enraged · Enthusiastic · Envious · Euphoric · Exasperated · Excited · Exhausted · Exhilarated · Fearful · Fondness · Frustrated · Grateful · Grief-stricken · Grumpy · Guilty · Happy · Hateful · Helpless · Hesitant · Hopeful · Hopeless · Horrified · Hostile · Humiliated · Hurt · Hysterical · Indifferent · Infatuated · Inferior · Insecure · Insulted · Interested · Intrigued · Irritated · Isolated · Jealous · Joyful · Liking · Lonely · Love · Lust · Melancholy · Neglected · Nervous · Numb · Optimistic · Outraged · Overwhelmed · Panicked · Passionate · Pity · Pleased · Powerless · Preoccupied · Pride · Proud · Receptive · Regretful · Rejected · Relaxed · Relieved · Remorseful · Resentful · Restless · Revulsion · Sad · Safe · Satisfied · Scared · Scornful · Self-confident · Self conscious · Shamed · Shocked · Shy · Sorrow · Spiteful · Stunned · Suffering · Surprised · Suspicious · Sympathy · Tender · Tenderness · Trust · Trusting · Uncertain · Uncomfortable · Vengeful · Weary · Worried
That’s a lot of possible answers to the question of how you feel right now. Language allows us to name emotions, but it doesn’t teach us much about what is underneath. If I am am Fearful, am I Afraid? Anxious? Panicked? Scared? Are there any real differences in how we feel when we describe ourselves with one or another of these words?
Assessing Mood or Emotion in Other Animals
It would be splendid if when we talked to the animals, and asked them how they were feeling, they would reply. If they can’t speak, maybe they could just send an email or tweet. But animals just don’t reveal many emotions. That doesn’t mean they don’t experience them. But without facial expressions that we understand, how can we know what another animal is feeling — or even if it has feelings?
Researchers in London5 recently did several very interesting cognitive bias tests with bumblebees. First, they trained the bees to enter a small box and fly to a blue placard above a tube. In that tube was a sugar solution that would reward the choice. The bees also had a chance to learn about a green placard marking a tube which contained only water. Once they learned to choose the tube with the blue placard, the time they took to perform this feat was measured and recorded. Now, some of the bees were given some sugar water in the tunnel leading to the box, and were timed as they went off to a placard on the other side of the box. But this time, the placard was not blue, not green, but blue-green. Bees that had received the sugar water got to the new placard faster than those who were not given the sugar water. The effects of sugar water on speed to reach the target was considered a “positive judgment bias in response to ambiguous stimuli and attenuated response to negative stimuli.6”
Was this just a sugar high that was powering the speedier bees? No. The researchers found that after the initial taste of sugar, the thorax temperature went up, but activity level remained the same. Bees that got sugar water flew no faster than those who got only water. Their earlier arrival at the correct placard was a consequence of a faster decision.
In another experiment, the researchers gave some bees sugar water, and other bees just water, and then held them in the tube for 10 seconds. At the end of this wait, the bee was squeezed by a device that held it in position for 3 seconds, the way a spider might ambush it. After this brief trauma, the bees were released and their time to start foraging was recorded. The bees who had started with sugar water began foraging more quickly than those who had not. This same effect has been found in humans, where sweet food increases positive emotions, improves negative mood, and reduces crying in newborns when they have been presented with unpleasant stimuli.7
What underlies the positive emotions that these bees experienced when they received the unexpected sugar water at the start of the experiment? It appears to be our friend dopamine, because when a dopamine antagonist (a substance that blocks the effects of dopamine) was given to the bees who were also given sugar water, the bees behaved as if they had received unsweetened water. Bees that only received unsweetened water as well as the dopamine antagonist did not differ from those given only unsweetened water, so it doesn’t seem that the antagonist slows things down, but rather just cancels the mood-lifting effects of dopamine.
In other research, a starling was trained to flip a white cardboard lid to be given a palatable mealworm (injected with water), and receive an unpalatable mealworm (injected with quinine) when a gray lid was flipped. Once the bird understood the trick (lifting the white lid and ignoring the gray lid), he was given a lid intermediate in color between the white and gray lids, and allowed to decide what to do. Starlings who were caged in an enriched cage, with lots of opportunity for play (natural branches varying in thickness, at different heights and angles, water baths, and a tray of chipped bark), were likely to flip the intermediate, ambiguous lid, showing a positive cognitive bias (they think this intermediate color is close enough to produce a tasty mealworm.) But starlings that had been moved from an enriched cage to a standard, boring cage showed a negative cognitive bias — they guessed that this intermediate color will produce no tasty mealworm.8
In humans, we normally have a positive cognitive bias — we are biased toward positive events. We are more attentive to them, learn them more easily, memorize them better, and expect them more often. My first book explored this thoroughly.9 While a positive cognitive bias might be the norm, a negative cognitive bias is possible. With such a bias, we are in a bad mood, and we are more attentive to negative events, learn them more easily, memorize them better, and expect them more often. There is a big difference in the world we see through these two biases — at least the difference between a glass half full and a glass half empty.
Animals likely have good moods and bad, positive and negative cognitive biases.
From these simple studies, we know that bumblebees and starlings are capable of experiencing happiness, optimism, and pessimism. My guess is that what happens in bees happens in starlings, and what happens in Vegas stays in Vegas.
We should not be surprised by these findings about the birds and the bees. It is known that their reward systems are similar to ours in a number of ways, and involve some of the same neurochemicals.10 Dopamine is known to be involved in reward-related processes,11 provides motivation for reward12, and that it affects arousal in both vertebrates and invertebrates.13 Even in nematodes (tiny round worms less than a tenth of an inch long) which dine on bacteria, dopamine guides the job of finding food14. Even nematodes must enjoy their dinner. Dopamine (and related neurochemicals, such as octopamine in the octopus) must date back to the dawn of behavior.
The judgment bias test used on the bees and starlings in these experiments has been used (with obvious variations) on many species recently15. Prior positive experience leaves the animal expecting good things. When in a good mood, an animal in this test often regards the ambiguous stimulus as positive, whereas the bad mood guides them to see the same stimulus as negative. The hopes of bees and starlings are not much different than the hopes of snakes,16 dogs,17 goats18, horses or humans.
Mapping Mood to Physiology
Because mood — by definition — has a biological counterpart but not a cognitive component, our thinking about mood is improved if we think a bit about the underlying biology. If we can identify a biological state that is common to those humans who experience some mood, then if we can find that state in another human, we could conclude that they are feeling the same. And if we find that biological state in another animal, such as a horse, we can draw the same conclusion.
A shared biology
It is fortunate for this line of reasoning that all of the neurotransmitters found in humans are also found in all other animals.19 We now know that a given neurotransmitter has similar effects across species studied. Until we are shown otherwise, we might believe that neurotransmitters and hormones were invented back when man looked like a jellyfish, and that they have come along through the millennia. If their effects are common across the current species studied, then we can imagine that the ancient species which must have shared them must have also been guided by the same neurochemical and hormonal forces. So understanding the joy of sex in a horse is not so hard if we have studies of it in a cow or sheep or human.
Consider the octopus. All of the hormones found in humans are also found in the octopus — an animal with three hearts, nine brains, eight legs, and blue blood. When a female octopus of breeding age meets a male (octopus), her estrogen level spikes, as does his testosterone level. When she guards her eggs, her body is high with a hormone that is nearly identical to oxytocin: cephalotocin. Researchers have found progesterone in female octopus, and corticosterone in both male and female octopus.20 An animal that is much different than us turns out to be much the same.
The origin of the oxytocin/vasopressin signaling system is thought to date back more than 600 million years. All vertebrate oxytocin- and vasopressin-like peptides have presumably evolved from an ancestral vasotocin by gene duplication. Today oxytocin/vasopressin signaling systems are found in vertebrates, including mammals, birds, reptiles, amphibians, fish, molluscs, annelids, nematodes and arthropods.21
If we can link ourselves to the octopus through a knowledge of the effects of estrogen, testosterone, progesterone, oxytocin, and corticosterone, if we understand that these hormones are produced under similar circumstances, and if we know what it feels like when one of these surges takes place, then surely we can know something of what it feels like when that same compound surges through another human, a horse, an octopus, or most any other animal. Do horses feel good after sex? Why not? If they did not, why would they do it?
For horses, we know what neurochemicals are available. And since they have none that we don’t have, and we have none that they don’t have, we are in a mighty good position to understand how a horse can feel — if only we would let ourselves.
Mood and Consciousness
Does an animal have to have consciousness in order to have a mood? I don’t think so, for several reasons:
I’ve said that mood comes from our biology, and has no cognitive component. Consciousness is cognitive. By definition, mood does not require consciousness.
Consciousness is probably required for verbal communication. But we don’t have to talk about a mood to experience it.
Neurotransmitters and Hormones
A neurotransmitter (neuropeptide) is a chemical messenger that is produced in the body at the ends of nerves in the sympathetic nervous system. They are protein-like molecules made from two or more bonded amino acids.
These messengers bridge the gap between one nerve cell and another, or between one nerve cell and a muscle or gland cell. Their signaling is done with electrical impulses. They carry information very rapidly through the body, but their effects are brief. Neurotransmitters are involved in everything we do. They make the heart beat, the lungs breathe and the stomach digest. When a muscle contracts, we can thank a neurotransmitter. When we feel good, we can thank a neurotransmitter.
A variety of chemicals function as neurotransmitters. Before they are needed, small quantities are stored in small round chambers in the signaling end of a nerve. When a neurotransmitter is activated and the nerve containing it is fired, it is secreted into the tiny gap — the synapse — between the signaling end of a nerve and the receiving end of another nerve. The neurotransmitter closes this tiny gap and binds to the receptors on the next nerve or muscle.
Several different kinds of neurotransmitter are involved in creating feelings of happiness. These organic chemicals are endogenous — created by the body — but can also be synthesized in a laboratory. They include signaling agents such as dopamine, morphine-like substances such as endorphins, chemicals that produce feelings of trust or love, such as serotonin and oxytocin, and chemicals that make us feel good when their levels are reduced, such as cortisol.
There are now over 60 known neurotransmitters and hundreds of subtypes of them. The literature is extensive and opaque, and this discussion is very, very simplified.
A hormone is a chemical messenger that is produced by the adrenal glands and released into the blood stream. Their signaling is done by chemical impulses. They carry information through the body more slowly than neurotransmitters, but their effects can last longer. A neurotransmitter has a small nearby target, such as the cells connected to a single nerve. A hormone will usually affect many cells, often in a distant target.
Some hormones are tremendously important in social behavior. In vertebrates and many invertebrates, the gonadal steroids estrogen and androgen influence communication, reproductive behavior (especially parental care and sex), agonistic actions such as aggression and predation, and affiliative behaviors including social play.22
A single chemical compound — such as epinephrine, oxytocin, vasopressin, and ADH — can be used both as a neurotransmitter and a hormone. As a neurotransmitter, such a chemical is created and stored in a nerve cell, and secreted when that nerve is fired. As a hormone, the chemical is created by the adrenal glands and released into the blood stream. As a neurotransmitter, it has a localized effect. As a hormone, it has a global effect.
Adrenalin (also known as epinephrine) is an example of a compound that operates both as a hormone and a neurotransmitter. When it acts like a hormone, it has been released into the bloodstream by the adrenal glands. When it acts like a neurotransmitter, it has been produced by a nerve ending, and is used to carry an electrical impulse to some target cell.
Neurotransmitters and Hormones that Underlie Mood and Emotion
Cortisol is a hormone produced by the adrenal gland. It gives a feeling of anxiety, interferes with sleep, and its level rises when we feel danger or stress or simply low blood sugar. I suspect that the rise of cortisol is triggered by the situation, and causes those feelings of danger or stress. When the cortisol level goes down, we feel good. I suspect it is released when a horse is separated from his herd, or when any social animal is separated from others. When an animal loses in combat for status in a group, its cortisol level goes up, and remains up, while the winner’s cortisol level drops (see the sections on Leadership, Respect, and Dominance). Massage has been shown to decrease cortisol levels.23 Cortisol increases blood sugar, suppresses the immune system, aids in the metabolism of fat, protein, and carbohydrates, and diminishes bone formation.
In the brain, dopamine works as a neurotransmitter that controls movement and posture, modulates mood, and plays an important role in both positive reinforcement and dependency. It also affects attention, learning, and pleasure.
The brain contains several dopamine pathways which are involved when we are motivated by a reward, when we meet a goal, or when drugs or alcohol make us feel intoxicated. Dopamine underlies both addiction and the effectiveness of positive reinforcement. Operating in the reward circuit, dopamine is released to produce pleasure — a global reward signal. Dopamine works in the brain to influence the operation of the nervous system.
Beyond pleasure, dopamine is involved in learning with a reward prediction error signal: when a reward is unexpected, or greater than expected, the signal contains this information.24 The unexpected reward might occur during clicker training, when the click is unexpected, dopamine is released, and associations are formed. The reward that is greater than expected is the jackpot, when the trainer gives a double treat or extra praise in response to a very good performance.
When continuous reinforcement has been used, so that your horse always expects the carrot slice when he does the trick, and you shift to partial reinforcement, you choose to not reward some occurrences of the trick. When this happens, the reward prediction error signal does not occur, and dopamine release drops below its normal level. When your horse finally gets a reward, he also gets a dopamine surge.
Dopamine works as a local chemical messenger outside the central nervous system. Blood vessels, the kidneys, the pancreas, and the immune system all produce dopamine, with effects ranging from increasing urine output in the kidneys, reducing insulin production in the pancreas, and increasing vasodilation in blood vessels. Except for the dopamine found in the blood, dopamine outside the brain is locally produced and has local effects.
Depression can result from reduced dopamine levels25; anti-depressants such as Zoloft and Prozac mimic the effects of dopamine, as does both chocolate and crystal meth. Massage has been shown to increase dopamine levels.26
Endorphins — Endogenous morphine — are a morphine-like substance that the body produces. The are “endogenous opioid neuropeptides” found in the neurons of both the central and peripheral nervous system. Endogenous simply means that they are produced by the body. Opioid means that they are opiate-like, acting on opioid receptors to produce morphine-like effects. By definition, endorphins are those neurotransmitters whose effects are suppressed by naloxone, a drug used with opioid overdoses.
Endorphins are likely involved in analgesia (pain reduction), reinforcement, cognitive function and motor integration. They create feelings of well-being.
Released when we are stressed, fearful, or in pain. Masks pain by binding to opioid receptors and activating them, inhibiting pain signals. Responsible for the euphoria of a runner’s high. May also be stimulated by laughter. Heroin, morphine, and marijuana mimic the effect of endorphins. Scents such as vanilla and lavender trigger endorphin release. Laughing, listening to music, eating chocolate, having sex, and taking a group exercise class may all release endorphins. Massage has also been shown to increase endorphin levels.27
Scientific understanding of endorphins is still emerging, but at this writing, the most important of the endorphins is Beta-endorphin — an endorphin created in the hypothalamus and the pituitary gland. It binds to the opioid receptors — the same receptors that bind to chemicals extracted from opium, such as morphine. Beta-endorphin works as an analgesic, released when the body is injured, numbing or dulling pain and helping the body feel better immediately. It is also released during exercise, and is the basis of the runner’s high. Beta-endorphins have been associated with significant improvements in depression.28 An injection of beta-endorphins may produce hypothermia.29
There are four other important endorphins: alpha-endorphin, beta-endorphin, gamma-endorphin, alpha-neoendorphin, and beta-neoendorphin. Alpha-endorphin is very similar in composition to Beta-endorphin, but hasn’t received the research that beta-endorphin has, and may be less important. It may inhibit the dopamine response, and have effects opposite to those of Gamma-endorphin.30 Gamma-endorphin is an endorphin that is identical to alpha-endorphin except that leucine is added to the end. As with alpha-endorphin, little is known about its exact role It may have anti-psychotic effects, and may hep regulate blood pressure. An injection of gamma-endorphins may produce hyperthermia.31 Alpha-neoendorphin and beta-neoendorphin are additional endogenous opioid peptides, about little is known.
Estrogen is the primary female sex hormone. It is responsible for the development and regulation of both the female reproductive system and secondary sexual characteristics. Because estrogen is found in all vertebrates and some invertebrates,32 we know that it has an ancient history.
This hormone has three important effects on a mare’s courtship. It increases her willingness to approach a male and induces solicitous behaviors. It improves the mare’s attractiveness to a stallion either directly or through the production of odors, pheromones, and vocalizations. And it primes for progesterone (see below).
Oxytocin is both a neurotransmitter and a hormone. As a neurotransmitter, it is created in a nerve cell. As a hormone, it is created in the hypothalamus and released by the pituitary.
The most important of all bonds is probably the connection between mother and infant. During coitus, when giving birth, and during breast feeding, there are surges of oxytocin in a mom, triggering feelings of love for the unborn. Mothers of all species may experience oxytocin surges at such times, though this is a broad claim, and the role of oxytocin in most species has not yet been studied.
Neurochemicals that belong to the vasopressin/oxytocin family are available in invertebrates such as the fruit fly,33 the silkworm moth,34 and the octopus35. The oxytocin in our bodies probably reached this exact form in early fish,36 and is now found, in some form, in all vertebrates (fish, amphibians, reptiles, birds, and mammals).37 In all species studied (such as frogs, toads, green turtles, caimans,38 snakes,39 and goats40) it has a similar structure and function.41 What we learn about its effects in one species can generally be applied to other species.
You’ll see in this book that oxytocin is my favorite hormone and neurotransmitter, because it triggers feelings of love and attachment.
The hormone oxytocin makes us feel good when we are together, and plays an important role in attachment and bonding42. It is likely that the oxytocin plays a big role in making our horses happy to be together and trust each other. It helps build the bond between mare and her foal. Cortisol makes us unhappy to be apart. When we get together, our oxytocin levels go up, and our cortisol levels go down. Proximity is rewarding, and separation is punishing. Evolution might have created the herding impulse with these two chemicals.
Oxytocin is produced in the hypothalamus and released by the pituitary. It is released during bonding, kissing, hugging, sexual reproduction, both during and after giving birth, and during nursing. It should be released in both of you when you hug your horse or he nuzzles you.
Bonding. Oxytocin gives a feeling of friendship, love, deep trust. Its effects last longer than those of dopamine. Oxytocin likely contributes to a mare’s love of her foal, your fondness of your horse, and your horse’s fondness of you.
Oxytocin helps develop and maintain our bonds with our mates in a few different ways. First, oxytocin facilitates approach behavior among men and women.43 Then, oxytocin promotes attraction and the formation of bonds in human men and women.44 Oxytocin levels are higher in new lovers than in single people, and these high levels may last for six months or more.45
One study found that men who were in monogamous relationships and were given an oxytocin nasal spray kept a greater distance from attractive women during a first encounter, an effect not found with single men or men in the placebo group.46 So oxytocin helps maintain fidelity once a monogamous relationship is established.
Having helped in establishing a relationship, oxytocin also plays a role during sex. It goes up, for sure, after sex.47
Oxytocin is important during birth, triggering uterine contractions during labor. When either the vagina or cervix are stimulated, oxytocin is created.48 Oxytocin levels peak at about the time of delivery, promoting a sense of euphoria in mom, and helping build a bond with her baby.49 Oxytocin is accompanied by some of our other favorite hormones, including endorphins which help keep pain under control.
Oxytocin is involved with milk ejection during lactation. “Milk ejection comes about because of a reflex, set up by the baby’s mouth sucking on the nipple. The nerves from the breast carry this stimulus to the brain, where it activates a group of very special nerve cells. These cells make oxytocin, which is then released, via the pituitary gland, into the blood, and travels to the breast. The breast has special muscle cells that respond to oxytocin by contracting, thus expelling the milk. It all happens rather fast.50”
Milking a cow is something that I can do, and it seems to work the same way. Provide her with a quiet, comfortable, familiar environment. Play her favorite music on the radio. Gently wash her udder with a warm wet washcloth. Now gently squeeze and pull each teat. Mrs. Cow’s oxytocin makes a squirt of milk, a second later.
This splash of oxytocin brings on a sudden feeling of contentment and pleasure as you breastfeed, I am told, and that encourages more contact with your baby. According to Gale Pryor, “breastfeeding guarantees that you and your baby will be in close physical contact 8 to 18 times in every 24 hours. In fact, nursing mothers tend to be with their infants altogether more than other mothers. In the first 10 days after birth, nursing mothers hold their babies more than bottle-feeding mothers, even when they are not nursing. They rock their babies more, speak to their babies more, and are more likely to sleep with their babies.51” All of this builds the bond between baby and mom. Thank you, oxytocin!
Oxytocin is important in the bonding between mom and baby. Take a ewe who has never given birth, and who is not pregnant. Let her stand in a paddock with a lamb and a small pile of hay. Give her a choice of what to do, and she heads for the hay. Give her a squirt of oxytocin in the brain, and she forgets the hay, heading straight to the lamb and mothering it.52 Oxytocin activates maternal behavior and bonding with babies.
Social Skills. Oxytocin seems to improve our social skills, increasing social behaviors such as trust,53 empathy,54 generosity55 and eye gaze detection.56 But its effects are not always positive. In a situation in which a human player lost more than others in a game, or won more than others in a game, oxytocin increased envy in the losing condition, and gloating in the winning condition.57 And there seem to be effects of upbringing. In one study, after a puff of oxytocin, men who had good relations with their mothers remembered them more positively, while those with poor relations remember them as even more negative and difficult. In another study, women were harshly disciplined as children were compared with women who had a more pleasant childhood. When given a squirt of oxytocin, the two groups of women behaved differently when they heard a recording of a crying baby. After a tough childhood, oxytocin is not guaranteed to create warm, gentle interactions.58
Oxytocin may have similar effects in men and women, but they are not identical. For example, one recent study found that oxytocin improved the perception of social interactions in both men and women, that oxytocin improved kinship recognition in women (but not men) and improved competition recognition in men (but not women.59) In another study, researchers found that men who received oxytocin behaved more aggressively toward competing out-groups than those in their in-group.60 Most studies of oxytocin have ignored the variable of sex, and while there is likely more to be discovered about sex differences in its effects, the main effects of oxytocin on males and females seem very similar. Because researchers learned about the connection between pregnancy, lactation, breast feeding, and oxytocin before learning about other oxytocin effects, oxytocin was once considered a “female hormone.” But no longer. Scientists now know it operates just fine in men.
Oxytocin levels are also raised by estrogen pills, apples, ginger, plums, wheat, tomatoes, chick peas, garlic, oregano, chocolate, snuggling with pets, a warm bath, soothing music, and oxytocin nasal spray. Massage has also been shown to increase oxytocin levels.61
Social Structure. Berkovitch and Deacon (2015)62 have provided a succinct summary of matriarchy in giraffes: “Giraffe cows seem to initiate bonding with their calves at birth, even if the newborn is dead.63 Most likely, such a social mechanism is founded upon a common mammalian neuroendocrine pattern involving elevated oxytocin levels around the time of parturition,64 which function not only to facilitate uterine contraction, but also to foster bonding between mothers and offspring.65 Indeed, the giraffe maternal relationship with offspring continues into adulthood, with unrelated adult females less likely to form herds than are mothers and their adult daughters.66” Deer, elk, elephants, and horses all behave like giraffes, albeit with shorter necks.
Progesterone is a hormone and key player in guiding the menstrual cycle, pregnancy and the development of embryos in humans and other species.67 Progesterone is also a building block of other sex hormones, and is important in brain functioning.
This hormone has a several effects on courtship. When it is on the rise after priming by estrogen, the mare’s sexual receptivity increases. But the prolonged secretion of progesterone inhibits sexual receptivity and helps maintain pregnancy.
Serotonin is a neurotransmitter found in the gastrointestinal tract, in blood platelets, and throughout the central nervous system of all animals. Serotonin gives humans feelings of pride, of well-being, of happiness, and of being loved. It affects mood, sleep, appetite, impulsivity, aggression. We must assume that if Serotonin does this for us, it must do this for other animals, and that an octopus, bird, or horse can have these same feelings.
Serotonin can affect mood, social behavior, appetite, digestion, sleep, learning, memory, and sexual desire. Imbalances in serotonin can result in depression, suicide, impulsive behavior, and aggressiveness. Drugs like LSD, PCP, and Ecstasy mimic the effects of serotonin.
Serotonin is a contributor to feelings of well-being and happiness.68 Serotonin is found in all animals. In insects, it has roles similar to those it has in humans, affecting memory, appetite, sleep, and behavior.69 When serotonin levels in locusts rise, they transform from a solitary life to a gregarious state.70
Serotonin is not limited to animals. Serotonin derivatives have been found in at least 16 different plant species.71 These derivatives help plants defend against pathogens72 and provide them with therapeutic benefits.73 In rice plants, serotonin has been found to be triggered by aging, and to inhibit it through creation of anti-oxidants.74 We benefit when plants and animals are made of the same stuff that we are. It wouldn’t hurt for us to acknowledge this.
In the GI tract, serotonin regulates intestinal movements, increasing motility. The central nervous system can also produce it with specialized neurons, where it helps regulate mood, appetite, and sleep. Learning and memory are both enhanced with serotonin — helping explain why positive reinforcement is so effective.
Serotonin derivatives have been implicated in fighting atherosclerosis,75 inflammation,76 tumors,77 bacteria,78 and stress.79 They may also be involved in reducing depression and anxiety. Serotonin even helps with wound healing. It works its way out of tissues and into the blood, where it is taken up by blood platelets and stored. When a wound occurs, the platelets on the scene release their serotonin, constricting blood vessels and helping with clotting.
Massage has been shown to increase serotonin levels.80
Testosterone is the main male sex hormone. It has a variety of useful effects on courtship and reproduction. Its greater availability in stallions than in mares contributes to greater size and strength of stallions, which they find useful in defending their herd and which the ladies may find attractive. When it increases in the spring, it primes a stallion for sexual adventure; when it decreases a short while later, a lower level helps diminish sexual interest and allow his band to get back to business. After a stallion ejaculates, a mare experiences a spike in testosterone, endorphin, and oxytocin levels. For a prospective fetus, this makes the internal environment more conducive to conception. For both stallion and mare, a surge in oxytocin is always a good thing, stimulating feelings of love, desire and care.81
Vasopressin is a hormone found in most mammals. It normally contains arginine, and is sometimes called arginine vasopressin. Most of vasopressin is stored in the pituitary before it is released into the bloodstream. However, some vasopressin may also be released directly into the brain, and accumulating evidence suggests it plays an important role in social behavior, sexual motivation and pair bonding, and maternal responses to stress.
In the previous section, I’ve focused on hormones and neurotransmitters that appear to be important in mood and emotion. There are many other messengers that play other roles in the body. For example, Acetylcholine is a neurotransmitter that affects movement, learning, memory, and REM sleep. Epinephrine is a hormone and neurotransmitter (and medication) that affects metabolism of glucose and energy release during exercise. GABA is the chief inhibitory neurotransmitter. It reduces neuronal activity and helps regulate muscle tone. Glutamate is a neurotransmitter active in areas of the brain involved in learning, thought and emotion. It is abundant in the body, and is used in over 90% of synaptic connections to the brain. Norepinephrine is a neurotransmitter that affects eating, alertness, and wakefulness, and mobilizes the body for action.82 There are over 100 other known neurotransmitters.83
Neurotransmitters and Hormones in Action
Neurotransmitters and Massage
Studies have shown that massage increases oxytocin, reduces the level of adrenocorticotropic hormone (ACTH), nitric oxide, and beta-endorphin. It might be that the nature of the massage is less important than the contact itself: oxytocin is released in response to physical contact in mice.84
We know that we feel good during and after massage, and studies attribute these good feelings of euphoria to the chemical messengers that massage produces. We find that massage raises the level of dopamine, endorphins, serotonin, and oxytocin, and lowers the level of cortisol in both humans and horses. Because these changes produce euphoria in humans, we should assume that similar changes in these compounds produce similar euphoria in horses. Massage feels good whether you are horse or human.
What is it about massage that triggers these chemical changes? Low frequency stimulation of peripheral nerves done through static touching (contact without motion) or stroking (moving touch) likely triggers the signals that produce these opioids.
The horse’s interpretation of the situation is very important in determining whether touch feels good or not. Until he relaxes, your touch may be a source of concern. Rhythmic and/or circular motions may be more soothing than random motions. Stroking with the grain of the hair will feel better than against the grain. Because nerves will habituate to an unchanging touch and stop firing, you’ll do better with stroking than with a static touch. Your strokes can be accompanied by warmth and by some gentle pressure. Once your horse determines that you are working to make him feel good, he will relax, and he’ll begin to show the signs of drowsiness.
For all of the benefits of touch, our society has blundered away from it recently, for fear that a school, a teacher, a scoutmaster, or a grandfather will be accused of inappropriate touch. For a great review of the value of touch, see Tiffany Field’s book on the subject.85
There are other means of using chemicals to generate feelings of well being and happiness in your horse. Turning on some soothing music in the barn, giving your horse a warm bath, and toweling him dry will likely do the job, raising his oxytocin levels with the music, warmth and the contact.
Neurotransmitters and Grooming
We could expect that because grooming is very similar to massage, that there would be similar roles for neurotransmitters.
Oxytocin has been found to produce significant effects on pair bonding as well as on allopreening in monogamous songbirds.86 Oxytocin injected into the brain induces social grooming87.
Neurotransmitters and Stress Reduction
The “relaxation response” is the opposite of the stress response. When it occurs, heart rate, blood pressure, respiration rate, and brain activity all drop.88
The attachment of dog and owner has been show to affect the health of the owner89 (and I would assume the dog as well). In other studies, a partner that the subject is attached to is helpful in buffering the effects of stress.90 Spending time with your horse should reduce your stress level and his.
Neurotransmitters, Friendship, and Love
Tobias Esch and George Stefano91 have written “Love is a complex neurobiological phenomenon, relying on trust, belief, pleasure and reward activities within the brain, i.e., limbic processes. These processes critically involve oxytocin, vasopressin, dopamine, and serotonergic signaling. Moreover, endorphin and endogenous morphinergic mechanisms, coupled to nitric oxide autoregulatory pathways, play a role.” In simpler terms: love involves oxytocin, vasopressin, dopamine, serotonin, and endorphins.
Your dog gazes into your eyes. What happens next? One very nifty study looked at the oxytocin levels in dog owners before and after interacting with their dogs. Some owners — those who reported having a close relationship with their dogs — received longer gazes from their dogs, and produced more oxytocin. Those with weaker relationships with their dogs received shorter gazes and produced less oxytocin. Dog owners who were instructed to not interact with their dogs during the experiment showed no change in oxytocin. Your dog’s gaze seems to increase your attachment, and certainly increases your production of oxytocin.92
There is, in fact, a considerable literature connecting oxytocin, friendship, and love.
- The oxytocin concentration in cerebrospinal fluid is positively correlated with social behavior in rats and monkeys;93
- Oxytocin plays an important role in pair bonding94 and social affiliation and trust.95
- In humans, intranasal administration of oxytocin has been shown to calm depressive tendencies and anxiety.96
- Intranasal administration of oxytocin increased gaze specifically toward the eye region of human faces.97
- Plasma oxytocin concentrations in humans and dogs increase after interactions.
Please be aware that not all findings concerning the intranasal administration of oxytocin get published, and selective publication of the positive results may exaggerate its effects.98
It seems that friendship/love, and proximity, trigger the production of oxytocin, and that the presence of oxytocin strengthens the bond. When the parties involved are two humans, mutual friendship or love is strengthened. When the parties involved are two horses, or one horse and one human, mutual friendship or love is strengthened.
Fisher, Aron, and Brown (2006) have looked at the brains of subjects who were intensely “in love” using functional magnetic resonance imaging. They conclude “romantic love is one of the three primary brain systems that evolved in avian and mammalian species to direct reproduction. The sex drive evolved to motivate individuals to seek a range of mating partners; attraction evolved to motivate individuals to prefer and pursue specific partners; and attachment evolved to motivate individuals to remain together long enough to complete species-specific parenting duties… The neural mechanism for romantic attraction motivates individuals to focus their courtship energy on specific others, thereby conserving valuable time and metabolic energy, and facilitating mate choice.99” Much is involved in love, not merely a few neurotransmitters surging about. But it all happens inside, and may depend more on biology and chemistry than on religion or philosophy.
Neurotransmitters and Sex
Adrenal steroids, vasopressin, oxytocin, dopamine, and endogenous opioids as well as opiates and higher levels/pulses of nitric oxide (NO) are released during pleasurable activities like sexual behaviors.100
Neurochemistry and Temperament
Many behaviors in man and horse are regulated by various neurotransmitter systems, with each such system playing a certain role.101 Multiple temperament traits (such as impulsivity, sensation seeking, neuroticism, endurance, plasticity, sociability or extraversion) have been linked to neurotransmitters and hormone systems. These temperaments interact with socio-cultural factors to form “personality.” With a look at neurotransmitter systems found in horse and human, we should be able to learn something about the temperaments of the horse. We will remember that temperament+socio-cultural factors=personality, and so, in the absence of much of the “socio-cultural”, our search will likely lead to a better understanding of horse temperament, not horse personality. We will look more at a horse’s personality in the next chapter.
It would be great if some researchers would be guided by neuropsychology in trying to explore animal personality: there should be consistent behavioral manifestations of neurochemical actions. Such an approach was taken by Gray (1982) to produce two main factors: anxiety and impulsivity. These two traits are measurable in behavior and can be understood at a physiological level. Anxiety corresponds to susceptibility to punishment and its effects on the behavioral inhibition systems; impulsivity may correspond to sensitivity to reward.102 A very nice start in this direction has been made by Irina Trofimova and Trevor Robbins in a 2016 paper.103
Fear, Anger, Flight or Fight
My horse sometimes gets angry. Anger is not a mood. It is an emotion. It has a cognitive layer that provides a context, an explanation, a rationale. It is reasonable to ask someone why they are angry.
Fear and anger are both negatively valenced and accompanied by high heart rate and arousal. In both emotions, heart rate and systolic blood pressure (the pressure that occurs when the heart beats — the 120 of a reading of “120 over 80”) increase about equally (the effects of adrenaline), but differ in important ways.
- Fear seems to be largely handled by a flood of adrenaline (epinephrine), whereas anger involves both adrenaline and noradrenaline (norepinephrine).
- Diastolic blood pressure (the pressure in the blood vessels when the heart is resting between beats — the 80 of a reading of “120 over 80”) increases more during anger104 (the effects of norepinephrine).
- Fear dilates peripheral arteries, whereas anger produces a net vasoconstriction in major muscle groups, differentially elevating diastolic pressure.105
- Fear is high arousal of the sympathetic branch of the autonomic nervous system; anger is a strong arousal state of both the sympathetic and parasympathetic branches of this system. (The autonomic nervous system is a system that operates primarily below consciousness and that regulates things like heart rate, digestion, respiratory rate, pupillary response, sexual arousal, and urination.) The sympathetic nervous system is sometimes called the “fight or flight”, “quick response”, or “mobilizing” system, and the parasympathetic nervous system has been called the “rest and digest” and “feed and breed” systems.
Flight or fight are neither moods nor emotions. But both have a physiological basis, and both require a state of high arousal of the autonomic nervous system.
In the cardiovascular system, the heart rate, systolic blood pressure and blood flow to the muscles increase. At the skin, peripheral vascular resistance decreases, so that diastolic blood pressure is lowered. In the lab, such changes can be brought about by mildly threatening mental arithmetic106 (raising muscular blood flow by 300 percent) or the mere threat of shock107 (increasing heart rate by 15 beats per minute.) These changes, along with high arousal triggered by a rush of adrenalin, prepare the animal for fighting or fleeing in the same way that the body prepares for exercise. And the feelings that accompany flight or fight? They must be our friends fear and anger.
Happiness, Sadness, Anger, Fear, and Relaxation
Thirty five years ago, researchers at Yale108 explored some physiological differences between fear, anger, happiness, sadness, and relaxation. They asked their subjects to visualize each of these emotions during their tests, while they measured heart rate, systolic blood pressure, and diastolic blood pressure. Their results show that these feelings can be distinguished in the lab, without interviewing or looking at facial expression. As may be seen in the graph below, fear and anger are similar in having a high heart rate and systolic blood pressure, but fear has a much lower diastolic blood pressure.
Mean changes in heart rate (HR) and in systolic (SBP) and diastolic (DBP) blood pressure separately for the happiness (HAP), sadness (SAD), anger (ANG), fear (FEAR), control (CON), and relaxation (REL) conditions following seated imagery.109
Can biological measures, such as heart rate and blood pressure help determine whether two emotions are actually different, or determine how closely related each is? Yep. This important study found nice differences between happiness, sadness, anger, fear, and relaxation. We can’t ask our horse to visualize anything, of course. But the experiment I just described gives us some clues that emotion has a measurable physiological basis.
Happiness, Stress, and Sadness
Two researchers in Taiwan110 sought to determine whether four different emotions — neutral, happiness, stress, and sadness — could be distinguished from heart rate variability. Subjects were young adult males who had chosen music that they felt corresponded with these emotions. The experimenters told the subject which emotion was about to be presented, then presented flash cards of human facial expressions111 which corresponded to these emotions, and with each flash card, also played the corresponding music. The intent of the music and flash cards was to try to induce the emotion that the stimuli suggested. After each presentation, subjects filled out an emotional scale. During the entire procedure, an electrocardiogram recorded each subject’s heart rate. Sounds complicated, but wait until you see what they did to analyze this: they weren’t interested in heart rate, but in heart rate variability. To assess this, they used statistical techniques to extract time-domain features, frequency-domain features, Poincare plot features, and differential features between activated and baseline states. Mighty complex, but the information came only from the heart. After some mind-boggling math, the researchers were able to correctly recognize the emotional state of the subject in each test 90% of the time, using heart rate variability. Perhaps a change of emotion or mood really is a change of heart.
One day, I suspect, a refined pacemaker could be attached to a horse, and set to record heart rate variability. The computer within it might display emotions on its small screen, and we could read our horse. It wouldn’t need to be precise, because a lack of precision could be made up for by its honesty. We’d know he wasn’t acting. We’d know we weren’t confused by wishful thinking. We’d know he was speaking from the heart. And even someone who is not a horse whisperer could make a great horse listener.
Physiology and Other Emotions
A number of studies have found physiological correlates of emotion. All methods summarized in the table below confirm that there’s lots of measurable physical stuff going on underneath emotion. These studies are summarized in a table because their measures were more complex than the heart rate variability study described in the previous paragraph, and because I didn’t want you to fall asleep so soon.
|electromyogram, electrocardiogram, skin conductivity, respiratory changes112||joy, anger, pleasure, sadness||92%|
|electromyogram, blood volume pressure, skin conductivity, respiration, heart rate113||neutral, anger, hate, grief, platonic love, romantic love, joy, reverence||81%|
|rate variability, skin impedance114||sad, calm pleasure, interesting pleasure, fear||80%|
|electrocardiogram, skin temperature variation, skin electrodermal activity115||sadness, anger, stress||78%|
|electromyogram, electrocardiogram, respiration, skin electrical activity116||happiness, disgust, fear||62%|
At the moment, it looks like we are cooking gumbo. Even though the emotional ingredients were not standardized in the studies just mentioned, and even though the means of measuring these emotions were not standardized, still we find that the studies were pretty good at distinguishing one emotion from another. So hurray for Science! Hurray for ideas on how to measure our horse’s emotions!
By measuring humans with known emotions, measurement techniques can be developed and tested, and we can learn what something like happiness or fear looks like at the physiological level. Such measures can then be applied to our horses, and we should be able to infer emotion from those measures.
Arousal and Valence
We don’t need a list of words, we need a model that shows the relation between our emotions — particularly those emotions which we understand without a paragraph of accompanying text. Anger and fear are such emotions, some of these others — like guilt and jealousy — seem more like something for novelists.
A good model of emotions should consider the dimension of valence — positive and negative. Positive emotions include being excited, happy, relaxed, or calm. Negative emotions include being fearful, anxious, sad, or depressed. Remember that these words are just labels for something underneath, and you could toss in “elation”, “joy”, “heart break”, and other words that expressed the same ideas.
A good model of emotions should also consider the dimension of arousal — high or low. Fearful means more arousal than anxious, and both fear and anxiety mean more arousal than sad or depressed. Similarly, excited means more arousal than happy, relaxed, or calm.
A good model would show both dimensions. Here’s one such model, from Mendel et.al., 2010.117
Core affect shown on two dimensions.118
Whether or not some mood or emotional state is experienced consciously by some animal doesn’t much matter to me. That it is experienced is important. I want to keep my horse, my mule, the bird on my knee, and the birds in my yard all over on the right side of the figure above, where their experience is positive. Oh, yes. And my wife.
Arousal differences in mood are accompanied by a desire to move (high arousal) or to remain still (low arousal). We move more when we are in Q1 or Q4 than when we are in Q2 or Q3.119
Animals want to keep on the right side, too. They work to obtain rewards and avoid punishment. Rewards generally improve an animal’s fitness. When they occur, our animal moves into the quadrant labeled Q1. When rewards disappear, the animal may move back, toward Q3. The arrow between Q3 and Q1 suggests approach. The other arrow, between Q2 and Q4, suggests avoidance. Finding itself in Q4 will trigger flight or fight responses.
A position on the Q2–Q4 axis is principally determined by the perceived presence of danger or threat. There are surely underlying biobehavioral systems that trigger approach/avoidance and/or activation/inhibition.120
Feeling Good, Being Aroused, and Catching your Horse
Bud is a very young mule. At this writing, in his short time on earth, humans have only attempted to catch him in his pasture a few times. His lack of experience with this project has left him apprehensive. He simply doesn’t know what will happen to him if he is caught. So while he is a mellow, friendly guy in his stall, where he has had lots of human contact, he is more like a wild animal in his pasture.
Using the two dimensional model above, if I want to catch him in the pasture, I need him to move from Q4 to Q2. This requires two different efforts:
- I need to lower his arousal. I do this by walking slowly in his general direction, looking at the ground (or with my hand over my eyes), with my arms at my side and my fingers closed. If he moves back, I freeze. If he seems agitated, I may turn and slowly walk away a short distance, then stop. In no case do I raise an arm or show extended fingers.
- I need to increase his pleasure. So I offer him the feed in the bucket I’m carrying. I offer him carrots. When he will let me, I praise him and rub his neck. He seems to stress a little when I try to rub his face in the barn, so my hands stay away from his face.
Standing in his pasture with my feed bucket, Bud shows all the signs of an approach/avoidance conflict. He wants the feed, but doesn’t want to be caught. His distance from me tells me just how strong these two desires are relative to each other.
Yesterday, I told a trainer that Bud was behaving like a wild animal with this conflict. I have backyard deer that behave like Bud, approaching when I fill the feeders, but not daring to get too close to me. I have backyard birds that will sit on a feeder just filled, but will not sit on the one I’m filling. I have raccoons who will approach closely when others are eating from my hand, but won’t come all the way to do it themselves. Bud’s anxiety seemed familiar.
The trainer told me that Bud needed to respect me, and needed to look to me as a leader. I told the trainer that the raccoons in my back yard have learned to eat from my hand without ever deciding that I was a leader, without ever giving me one bit of respect. If I go outside and call them, some come running. Their reward activation system is operating in high gear. But they don’t need leadership.
I’ve resolved to work on catching Bud in the late afternoon, just before he comes into the barn. At that time, his yearning for grain should be higher than when he has just been turned out after breakfast, tipping his approach/avoidance conflict in my favor. I’ve resolved that my next few sessions won’t involve catching at all, but simply focus on grain delivery and neck scratches and rubs, and that when this comes easily, perhaps he and I will go for some short walks in his pasture.
And my raccoons? I won’t be saddling them any time soon. I think I’ll continue to let them sit on my bare feet on a summer’s eve, snack on cashews, and watch the world go by. Perhaps I don’t need to do anything about their need for leadership and their yearning for someone they can respect. And yes, I’ve had my rabies vaccine.
1 Image source: https://pixabay.com/en/emoticons-smilies-set-smiley-blue-150528/ via https://commons.wikimedia.org/wiki/File:Mood_and_Emotions.jpg
2 Montgomery, Sy. The soul of an octopus: A surprising exploration into the wonder of consciousness. Simon and Schuster, 2015. Pp 115-116.
3 Keltner, D., Lerner, J.S., 2010. Emotion. In: Handbook of Social Psychology.
John Wiley & Sons, London, pp. 317–352.; Scherer, K.R., 1984. On the nature and function of emotion: a component process approach. In: Approaches to Emotion. Erlbaum, Hillsdale, NJ, pp. 293–317.
4 This question is adapted from “Quizzes ‘n More!” Wisconsin Relationship Education. 2010. http://wire.wisc.edu/quizzesnmore/emotionwords.aspx
5 Perry, Clint J., Luigi Baciadonna, and Lars Chittka. “Unexpected rewards induce dopamine-dependent positive emotion–like state changes in bumblebees.” Science 353, no. 6307 (2016): 1529-1531.
6 Perry, Clint J., Luigi Baciadonna, and Lars Chittka. “Unexpected rewards induce dopamine-dependent positive emotion–like state changes in bumblebees.” Science 353, no. 6307 (2016): 1529-1531. Quote from page 1531.
7 Desmet, Pieter MA, and Hendrik NJ Schifferstein. “Sources of positive and negative emotions in food experience.” Appetite 50, no. 2 (2008): 290-301.; Fernandez, Mercedes, Elliott M. Blass, Maria Hernandez-Reif, Tiffany Field, Miguel Diego, and Chris Sanders. “Sucrose attenuates a negative electroencephalographic response to an aversive stimulus for newborns.” Journal of Developmental & Behavioral Pediatrics 24, no. 4 (2003): 261-266.; Macht, Michael, and Jochen Mueller. “Immediate effects of chocolate on experimentally induced mood states.” Appetite 49, no. 3 (2007): 667-674.
8 Bateson, M., and S. M. Matheson. “Performance on a categorisation task suggests that removal of environmental enrichment induces pessimism’in captive European starlings (Sturnus vulgaris).” Animal Welfare.16 (2007): 33.
9 Matlin, Margaret W., and David J. Stang. The Pollyanna principle: Selectivity in language, memory, and thought. Schenkman Pub. Co., 1978.
10 Perry, Clint J., and Andrew B. Barron. “Neural mechanisms of reward in insects.” Annual review of entomology 58 (2013): 543-562.
11 Barron, Andrew B., Eirik Søvik, and Jennifer L. Cornish. “The roles of dopamine and related compounds in reward-seeking behavior across animal phyla.” Frontiers in behavioral neuroscience 4 (2010): 163.
12 Perry, Clint J., Luigi Baciadonna, and Lars Chittka. “Unexpected rewards induce dopamine-dependent positive emotion–like state changes in bumblebees.” Science 353, no. 6307 (2016): 1529-1531.
13 Andretic, Rozi, Bruno van Swinderen, and Ralph J. Greenspan. “Dopaminergic modulation of arousal in Drosophila.” Current Biology 15, no. 13 (2005): 1165-1175.
14 Barron, Andrew B., Eirik Søvik, and Jennifer L. Cornish. “The roles of dopamine and related compounds in reward-seeking behavior across animal phyla.” Frontiers in behavioral neuroscience 4 (2010): 163.
15 Reviewed in Roelofs, Sanne, Hetty Boleij, Rebecca E. Nordquist, and Franz Josef van der Staay. “Making decisions under ambiguity: judgment bias tasks for assessing emotional state in animals.” Frontiers in Behavioral Neuroscience 10 (2016).
16 Couturier, Lisa. The Hopes of Snakes: And Other Tales from the Urban Landscape. Beacon Press, 2005.
17 Mendl, M., Brooks, J., Basse, C., Burman, O., Paul, E., Blackwell, E., Casey, R., 2010b. Dogs showing separation-related behaviour exhibit a pessimistic cognitive bias. Curr. Biol. 20, R839–R840
18 Briefer, E.F., McElligott, A.G., 2013. Rescued goats at a sanctuary display positive mood after former neglect. Appl.Anim. Behav. Sci. 146, 45–55.
19 I began the sentence with “It seems”. Surely this claim might be proven wrong, and “all species” might need to be changed to “most”. But I don’t know of any evidence that there is any species that lacks any of the neurotransmitters found in humans.
20 Montgomery, Sy. The soul of an octopus: A surprising exploration into the wonder of consciousness. Simon and Schuster, 2015. p. 115.
21 Gruber, Christian W. “Physiology of invertebrate oxytocin and vasopressin neuropeptides.” Experimental physiology 99, no. 1 (2014): 55-61.
22 Insel, Thomas R. “The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior.” Neuron 65, no. 6 (2010): 768-779.
23 Field, T., Hernandez-Reif, M., Diego, M., Schanberg, S., & Kuhn, C. (2005). Cortisol decreases and serotonin and dopamine increase following massage therapy. International Journal of Neuroscience, 115(10), 1397-1413; Field, T., Diego, M., Dieter, J., Hernandez-Reif M., Schanberg, S., Kuhn, C., Yando, R., & Bendell, D. (2004). Prenatal depression effects on the fetus and the newborn. Infant Behavior and Development, 27, 216–229.; Field, T., Sunshine, W., Hernandez-Reif, M., Quintino, O., Schanberg, S., & Kuhn, C. (1997). Massage therapy effects on depression and somatic symptoms in Chronic Fatigue Immunodeficiency Syndrome. Journal of Chronic Fatigue Syndrome, 3, 43–51.
24 Schultz, Wolfram. “Neuronal reward and decision signals: from theories to data.” Physiological Reviews 95.3 (2015): 853-951.
25 Delgado PL. Depression: the case for a monoamine deficiency. J Clin Psychiatry 2000; 61 Suppl. 6: 7-11; Delgado PL, Moreno FA. Role of norepinephrine in depression. J Clin Psychiatry 2000; 61 Suppl. 1: 5-12; Hirschfeld RM. History and evolution of the monoamine hypothesis of depression. J Clin Psychiatry 2000; 61 Suppl. 6: 4-6
26 Field, T., Hernandez-Reif, M., Diego, M., Schanberg, S., & Kuhn, C. (2005). Cortisol decreases and serotonin and dopamine increase following massage therapy. International Journal of Neuroscience, 115(10), 1397-1413.; Field, T., Diego, M., Dieter, J., Hernandez-Reif M., Schanberg, S., Kuhn, C., Yando, R., & Bendell, D. (2004). Prenatal depression effects on the fetus and the newborn. Infant Behavior and Development, 27, 216–229.; Field, T., Sunshine, W., Hernandez-Reif, M., Quintino, O., Schanberg, S., & Kuhn, C. (1997). Massage therapy effects on depression and somatic symptoms in Chronic Fatigue Immunodeficiency Syndrome. Journal of Chronic Fatigue Syndrome, 3, 43–51.
27 Kaada, Birger, and Ove Torsteinb. “Increase of plasma β-endorphins in connective tissue massage.” General Pharmacology: The Vascular System20.4 (1989): 487-489.
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29 Bloom, Floyd, David Segal, Nicholas Ling, and Roger Guillemin. “Endorphins: profound behavioral effects in rats suggest new etiological factors in mental illness.” Science 194, no. 4265 (1976): 630-632.
30 Nijkamp, Frans P., Jan M. van Ree, Jacq G. Nijssen, M. Versluis, and David de Wied. “Opposite interactions between α-and β-endorphin fragments with dopamine mediated responses on the rat rectum in vitro.” Naunyn-Schmiedeberg’s archives of pharmacology 321, no. 3 (1982): 213-217.
31 Bloom, Floyd, David Segal, Nicholas Ling, and Roger Guillemin. “Endorphins: profound behavioral effects in rats suggest new etiological factors in mental illness.” Science 194, no. 4265 (1976): 630-632.
32 Mechoulam, R., Robert Wayne Brueggemeier, and D. L. Denlinger. “Estrogens in insects.” Cellular and Molecular Life Sciences 40, no. 9 (1984): 942-944.; Ryan, Kenneth J. “Biochemistry of aromatase: significance to female reproductive physiology.” Cancer research 42, no. 8 Supplement (1982): 3342s-3344s.
33 Zheng, Yingcong, Birgit Hirschberg, Jeffrey Yuan, Alice P. Wang, David C. Hunt, Steven W. Ludmerer, Dennis M. Schmatz, and Doris F. Cully. “Identification of two novel Drosophila melanogaster histamine-gated chloride channel subunits expressed in the eye.” Journal of Biological Chemistry 277, no. 3 (2002): 2000-2005.
34 Gaojun, Zhang, and Tang Zhichun. “Effects of Oxytocin on Oviposition of Silkworm” Newsletter of Sericultural Science 2 (2000): 002.
35 Takuwa-Kuroda, Kyoko, Eiko Iwakoshi-Ukena, Atsuhiro Kanda, and Hiroyuki Minakata. “Octopus, which owns the most advanced brain in invertebrates, has two members of vasopressin/oxytocin superfamily as in vertebrates.” Regulatory peptides 115, no. 2 (2003): 139-149.
36 Acher R, Chauvet J, Chauvet MT. 1995 Man and the chimaera. Selective versus neutral oxytocin evolution. Adv. Exp. Med. Biol. 395, 615–627
37 Goodson JL. 2008 Nonapeptides and the evolutionary patterning of sociality. Prog. Brain Res. 170, 3–15.
38 The presence of oxytocin in frogs, toads, green turtles and caimans is reported here: Sawyer, Wilbur H., Robert A. Munsick, and H. B. Van Dyke. “Evidence for the presence of arginine vasotocin (8-arginine oxytocin) and oxytocin in neurohypophyseal extracts from amphibians and reptiles.” General and comparative endocrinology 1, no. 1 (1961): 30-36.
39 Perez-Figares, J. M., J. M. Mancera, E. M. Rodriguez, F. Nualart, and P. Fernandez-Llebrez. “Presence of an oxytocin-like peptide in the hypothalamus and neurohypophysis of a turtle (Mauremys caspica) and a snake (Natrix maura).” Cell and tissue research 279, no. 1 (1995): 75-84.
40 Linzell, J. L., and M. Peaker. “The effects of oxytocin and milk removal on milk secretion in the goat.” The Journal of physiology 216.3 (1971): 717.
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