“His examination revealed that [the patient] had no fever, no pain anywhere, and that his only concrete feeling was an urgent desire to die. All that was needed was shrewd questioning… to conclude once again that the symptoms of love were the same as those of cholera…”
[Gabriel Garcia Marquez]
‘Lovesickness’ is considered by some doctors, and sometimes their patients, to be a disease. The experience of lost, rejected or unrequited romantic love can provoke depression, sleeplessness, chest pains, loss of appetite, and various digestive disorders. Conversely, being in love can bring a state of elation and joy.
The euphoric feelings associated with ‘falling in love’ are produced by a chemical. Its name is phenylethylamine, and it is a natural amphetamine whose effects on our brain and nervous system are quite similar to cocaine. As a consequence, it may provoke addiction-like symptoms.
Phenylethylamine, along with other pleasure-inducing compounds such as dopamine and the endorphins, are used for communication between cells in all animals, plants, fungi and even bacteria. This implies that cellular life is chemically wired for ‘pleasure’.
During evolution these signals were co-opted for transmission and processing of complex information. In animals they have found a highly specialised role; to relay messages between nerve cells, and so serve as ‘neurotransmitters’. Finally, in ourselves and in mammals, they are associated with what we understand as ‘feelings’, or emotions, including love, safety and trust.
Whilst some mammals pair-bond for only a single breeding season, others mate for life. The way their (and our) neural systems use these pleasure-provoking chemicals has a profound influence on the strength of these bonds.These signals, referred to by Candace Pert as the ‘molecules of emotion’, entwine our whole body with the emotional experience. The sensations these molecules communicate allow us to ‘feel our feelings’ and to ‘make sense’ of the information they bring.
All primates are neurally hard-wired for social connection. Even so, humans are unusual. Our mirror neuron network, which interlinks with our emotionally responsive neural circuits, enables us to ‘mirror’ the emotional and physiological experiences of others.
This runs through all types of human interactions, direct or indirect, such as when we read, hear or think of the words and actions of others. Hence our emotions can arise independently of our immediate circumstances, such as when a distant memory suddenly surfaces or we anticipate a future event.
This difference underpins the distinctively human capacity to consciously craft enduring love relationships. Human romances may end when the initial phenylethylamine-associated euphoria passes, or may mature into a richer companionship, incorporating different forms of friendship, affection and intimacy. These various love interactions are co-created by the participants; each and every relationship between two human beings is unique.
Evolution suggests that, as in other animals, our emotional response system (including our capacity for ‘love’) is a behavioural adaptation that has been selected and refined across the aeons. This implies that our human capacity for ‘love’ has also evolved through selection, and accordingly might be an adaptation.
What are the effects of our emotions, and how do they adapt us to our environment? How did this mechanism evolve? And why does our human emotional experience seem so much more complex than that of other animals?
What are emotions?
The primary purpose of our brain, indeed of any brain, is to feel; ‘thinking’ is an ‘add-on’.
Emotions provide an instinctual, high-speed mechanism for processing incoming sensory information. The resulting response focuses our attention, and enables us to make risk-reward assessments of our situation.
In most cases this happens extremely quickly, shifting our physiology and behaviour before the higher brain circuits have yet registered the trigger of this change. Whilst ‘moods’ can last for days, our experience of fear, for example, can arise in less than half a second.
Comparative studies of humans and other mammals suggest that we share a repertoire of basic or ‘primary’ emotions. These reflexes allow us to respond rapidly to our changing circumstances. They keep us alive through the hazards of our day, manage the pace of our vital functions as we work and rest, and inform us instinctively about whom we can trust.
Opinions differ as to how best to define this emotional repertoire.
• Paul Eckman suggests that animals, particularly mammals, experience six basic emotions: fear, disgust, happiness, sadness, anger and surprise.
• To this list, however, Robert Plutchick adds trust and joy.
• In contrast, Rachael Jack, when analysing the emotional signals expressed in human faces, proposes we have only four primary feelings; happiness, sadness, fear/surprise (fast arousal) and anger/disgust (slower arousal).
• Elizabeth Kubler-Ross, studying humans, renders the full list simply as ‘love’ and ‘fear’, and suggests that all other experiences stem from these.
All agree, however, that these basic emotional responses are either positive or negative, and can vary in intensity from ‘mild’ to ‘very strong’.
In all cases, emotional responses are learned; mammals, vertebrates and even insects and other invertebrates imprint behaviours from their own direct experiences as well as observing others. This mechanism is highly flexible; an animal’s response varies according to the subtleties of its context.
For instance the fear responses of wildebeest vary according to the perceived density of their lion predators. Low levels of fear prompt these prey animals to increase their grazing intensity and reduce the amount of time spent hiding. Intense fear, triggered by only a small increase in lion numbers, might cause them to stampede. Emotions, then, instinctively adapt an animal’s behaviour to its immediate circumstances.
How do we ‘feel’ these feelings?
When we ‘feel’ something, we become aware of the current state of our body. Brain imaging studies show that we operate an emotional response in our lower brain circuits a fraction of a second before signals reach higher processing centres in the frontal cortex, and we begin to ‘think about’ what is actually happening.
These lower brain centres control the autonomic nervous system. The latter comprises two networks: ‘sympathetic’ and ‘parasympathetic’. Their names, reflecting a historical view of these systems as being ‘in sympathy’ and ‘in opposition’ to feelings, are in practice misleading.
The anthropologist Stephen Porges suggests instead that we consider these opposing neural networks as giving us our ‘autonomic state’. We perceive this physiological body state and interpret it as a ‘feeling’.
The sympathetic system ‘turns up’ our responses during emergencies and in states of positive excitement and anticipation. In contrast, feelings of calm, happiness and trust are under parasympathetic control, and are delivered primarily via the vagus nerve. In combination, these two systems provide our bodily experience of emotions across a spectrum from fear to love.
The vagus is the longest nerve in the human body. It runs from the brain to many of the organs, including the heart, lungs, liver and gut. Vagal impulses to these organs produce physical sensations of well-being such as a warm expansion in the chest, along with feelings of compassion, gratitude, happiness and love.
This is also a ‘mixed nerve’, acting as an ‘information highway’. Sensory information from the organs and tissues return back to the brain via the vagus. In particular the heart and the digestive system keep us informed of the overall state of our body. Both of these organs have a certain degree of neural autonomy; the heart generates its own rhythm, and the enteric nervous system produces local nerve impulses that drive the rhythmical contractions of smooth muscles around the gut.
We often talk about ‘gut feelings’, or ‘getting to the heart of the matter’. The digestive system is a major sensory organ, monitoring our interactions with the world through the food we eat. Our gut bacteria produce the bulk of our body’s neurotransmitters, and make many signals that affect our mood and emotions.
The heart’s abundant sensory nerves monitor these and other signals, sending information about our body state back to the brain. These messages are carried by the vagus directly to the amygdala and other components of the limbic system. These circuits process the data from our organs into information about ‘how we feel’, and present this to our conscious awareness.
Do other animals feel what we feel?
The vagus nerve makes us aware of our body state. This is true for all mammals, and to an extent is all vertebrates.
Emotional states of calmness and trust are produced by the parasympathetic nervous system and in particular by vagus nerve activity. When sensory vagal fibres perceive a calm body state, they promote the release of oxytocin from the brain.
This peptide (a short protein) signal, known as the ‘bonding hormone’ in higher vertebrates, has two roles. First it acts as a ‘neuromodulator’, increasing the activity of the pleasure-promoting dopamine-sensitive neurons in the central nervous system. Second, released into the blood as a hormone, it calms our body organs and reduces the level of arousal triggered by fear.
The heart and gut monitor the effects of oxytocin, and relay this information back to the brain via the vagus. This completes a neuro-chemical circuit which keeps the brain’s emotional centres informed of the state of our bodies, and enables us and other mammals to feel how and what we feel.
Oxytocin has many physiological roles in mammals including birth, nursing and the establishment of pair bonds. This signal is released in response to affection between parents and offspring and group activities such as grooming. It acts to increase the effect of dopamine-based nerve pathways and other pleasure-promoting neural circuits in the brain. In this way we learn to associate calm, shared social experiences with feelings of pleasure, safety, trust and ‘love’.
Social bonding is particularly intricate amongst the fruit-eating primates. Chimpanzees forage collectively for fruit, sharing the proceeds. Mutual grooming results in oxytocin production which provokes relaxation and pleasure in these animals. This promotes trust and cohesion within the tribe, enabling them to trust each other and cooperate with this task.
Juvenile mammals adopt the emotional response behaviours of their social group. Like us, they learn to associate the vagus-mediated bodily shift into a calm physiological state with the circumstances that accompany trust and safety. The feelings that we and other mammals feel when nursed by our mothers as infants help us to learn how to build strong social bonds and to engage in other forms of social intimacy.
In addition, humans can also experience more complex emotional states such as shame, guilt, and remorse. Our ability to experience these feelings is dependent upon our development of speech and language. To access our complex emotions and understand our feelings we draw upon specific words.
This is one reason why psychologists have traditionally considered that other animals do not have emotions. This opinion has changed; most researchers now believe that we share a basic emotional repertoire with all mammals. Unlike them, however, we cannot shut down our thoughts, and so we do not experience the simplicity of what they presumably feel.
How did these feeling responses evolve?
All animals show what we can recognise as an emotional response, at least to ‘fear’. As the vertebrates evolved, the autonomic response system increased in complexity and the development of the vagus nerve network became more elaborate. This has permitted an increasingly sophisticated regulation of the heart and respiration; controlling oxygen uptake in turn determines the body’s metabolic rate.
Stephen Porges proposes that the vagus has evolved through three stages, producing three autonomic ‘subsystems’ which supersede each other in delivering an increasingly sophisticated neural control of the heart and circulation. These subsystems support the physiological responses required for three types of adaptive behaviour.
i Primitive vertebrates such as the hagfish make passive avoidance (‘freezing’) responses to fear. Their slow (unmyelinated) vagal fibres connect limbic centres in the brain to the gut, shutting down digestion to conserve energy.
ii Higher vertebrates have a two-component oppositional autonomic system comprising a stimulatory (sympathetic) and calming (parasympathetic) function. This enables active avoidance (‘fight or flight’) behaviours. The increase in blood pressure that results from increasing sophistication in this system gave support to elaborated lung tissues, permitting the transition of vertebrate life onto land.
iii Porges’ third stage involves the autonomic system of mammals and birds being adopted and subsequently modified through evolution into an emotional response system that facilitates rapid social communication.
Like other mammals, most of our emotional responses are also social signals. We learn these responses as children, initially from the adults in our environment. Our social group has shared signals which relate to the experiences encountered in our specific situation.
All mammals accumulate unique neural wiring in this way. Adopting the social and other behavioural responses of their tribe enables juveniles to imprint the reactions which they need to survive in their ecological setting.
Sensory inputs may not initially provoke emotional responses in our infants. As they learn to associate for instance the smell of rotting food with our emotional reaction, they too begin to respond to this stimulus with disgust, and avoid it as ‘dangerous’. Conversely our and other mammal infants quickly learn to associate the scent and sound of mother with safety and trust.
Mammals and birds, the most emotionally sophisticated of vertebrates, also have the fastest nerve and muscle reactions. These rapid responses depend upon a stably regulated body temperature, which requires their autonomic system to maintain an adequate supply of food and oxygen to the muscles. These benefits are under the control of the autonomic nervous system. The increased basal rate of their metabolism, resting heart beat and respiration rate compared with other vertebrates is delivered by myelinated (insulated) fibres of their vagus network.
How have emotional responses enabled us to adapt?
Emotions trigger imprinting and deploying of strategic responses which tailor an animal’s behaviour to its specific survival needs. Higher vertebrates (just like some insects and other invertebrates) can perceive and adopt the behaviours of others in their environment. This enables effective behaviour strategies to spread within a local population. These various types of response are adaptations, and are selectable by evolution.
In the social vertebrates, birds and mammals, emotion has a further role; ‘feelings’ bond the tribe, building and maintaining close social interactions, making their group respond as a coherent unit. Here emotions function as a social mechanism enabling complex animal societies to function cooperatively. This has shifted their ecological unit of selection from individuals to groups.
Coupling the parasympathetic calming response with pleasure circuits produces a positive emotional state, such as experienced during our most intimate social interactions. Feeling safe to ‘keep still’ is also needed for pair-bonding and to allow for the physical proximity associated with seduction and passion.
Pair-bonding in mammals depends upon oxytocin and another closely-related peptide, vasopressin. Both sexes produce these two signals in varying amounts. Female mammals require a surge in oxytocin levels to bond with her mate, whilst her partner bonds in response to high vasopressin.
Stephen Porges believes that the vagus-mediated primitive, vertebrate ‘freezing’ response (fear-triggered immobilisation) has been co-opted in mammals for reproduction, nursing and pair bonding. He proposes that a synchronised release of oxytocin and vasopressin in combination could activate vagal and sympathetic responses in the body at the same time, generating an unique autonomic state of calmness with sexual arousal, supporting courtship behaviours which we might call ‘love’.
Courtship bonds in mammals and birds compel both parents to work together to look after their offspring. The majority of all vertebrates die as young juveniles. The selectable ‘pay-off’ for high parental investment may be an improved survival of these animal’s offspring during their most vulnerable life stage. The emotional bonds between parents and their offspring are crucial in motivating these adults to deliver this intense protection and care.
In mammals the vagus connects with other mixed cranial nerves (the trigeminal, facial and glossopharyngeal nerves) to control the structures used to vocalise, and in primates, to coordinate the production of facial expressions. These signals, along with posture and movement, communicate an animal’s emotional state to others. In humans, these neural connections are particularly advanced, and coordinate the many muscles that enable us to speak.
As in mammal calls, the emotional content of our voices are still discernible. The information is transmitted through the ‘rhythm and music’ (the prosody) of our words and phrases. We unconsciously register the emotional state of others whilst our conscious awareness is preoccupied with the meaning of their words.
Pleasure-associated grooming linked to vagal coordination of the voice may have provided our primate ancestors with the means to ‘groom’ each other using vocal sounds. A form of ‘vocal grooming’ may have been later co-opted into what became human speech.
Is our human experience different?
We experience a much greater complexity of emotional states than other mammals. Our understanding of ‘how we feel’ is dependent upon using words to define these emotions to ourselves, and share them as ideas.
Emotions code the intensity of close kin relationships and bonding between all social mammals. Our differences lie in the way that words can redefine our experience. Words equip us to distinguish our feelings from those of others, and so better understand the content of our own and others’ actions. This allows us to ‘make sense’ of our experiences.
Words are symbols. Unlike a picture or other sign, their meaning is not directly inferable. It is unclear whether human’s use of word symbols is absolutely unique. For example, dolphins use ‘signature whistles’ like names, to identify individuals in their pod. It is not clear however whether the repeated phrases of dolphins ever ‘tell a story’. In the human ‘tribe’, words such as ‘love’ are metaphors which elicit strong emotional responses when we think them. They engage us in a shared story about the idea they represent, bringing an even greater intensity to our emotional lives.
The emotional responses of animals are triggered by their external circumstances in the present moment. We can feel emotions in response to the contents of our thoughts in the absence of any direct external stimulus. We can, with equal ease, re-live both positive and negative past events, and even fear things which we may never directly experience, such as ‘snakes’, ‘bankruptcy’ or ‘terrorism’. These internally created stimuli can bring us heightened emotional responses of various kinds, from intense love to debilitating depression and anxiety.
Antidepressants such as Prozac (Fluoxetine) ‘damp down’ our unwelcome emotional extremes by indirectly modifying the action of neural circuits using dopamine. This can bring a welcome reduction in the severity of depression and anxiety symptoms. The same effect however applies to all our emotional responses. Some users of antidepressants report side effects of ‘emotional numbness’, and feelings of isolation and emotional distance from others.
Whilst ‘love’ and other emotions may be (as Stephen Porges suggests), a ‘by-product’ of the mammalian autonomic nervous system, the act of ‘giving love’ structures our whole society. Human language enables us to define our personal emotional state with high accuracy, and to acknowledge its complexity in our conscious and collected awareness. We use words to describe our feelings, code meaning into our experiences, share those experiences with others. Through our words and stories, we are constantly inventing and reinventing ourselves.
“He allowed himself to be swayed by his conviction that human beings are not born once and for all on the day their mothers give birth to them, but that life obliges them over and over again to give birth to themselves.” – Gabriel Garcia Marquez; Love in the Time of Cholera
Human ‘love’ then, is an emotional response, a neurochemical body state, an addiction, a behavioural reflex, a motivation, a consequence, and an idea with a story of its own. It is visceral, yet finds expression through our minds, and we recognise it through our own and other’s actions. We receive it by giving it away, and welcome it by caring for ourselves and others. It is universal yet indefinable, we experience it when we share it, and in each of our relationships it finds its own, unique expression.
- Emotions are a source of information about our immediate world; a fast mechanism for processing sensory information and providing us with a means of assessing our levels of ‘risk’, and ‘safety’. They result in rapid alterations in internal state, which have associated behaviours that are adaptive and assist with the survival of the animal.
- Emotions are a flexible adaptive mechanism for adapting an animal’s behaviour to its world. These behaviours are learned from the ‘tribe’. They ow us (and other mammals) to learn from experience and make better adapted future responses.
- We share a repertoire of ‘primary’ instinctual emotions with mammals. These responses may also be present in less sophisticated forms in more primitive forms of vertebrates, and indeed invertebrates. The sophistication of these responses appears to mirror the complexity of their sensory perceptions and neural networks.
- In vertebrates, the physical aspects of emotion are mediated through the autonomic (instinctual) nervous system. Changes in ‘autonomic state’ are and perceived in the body as ‘feelings’.
- The autonomic nervous system has evolved through three levels in the vertebrate clade, shifting the emotional response from a chemical (circulating hormone) mechanism to a neural process with two opposing functions (the sympathetic and parasympathetic nervous systems).
- The increased levels of sophistication of this vertebrate response system allow better control of body temperature, metabolic rate, and heart and circulation.
- In the mammals the vagus has a fast acting (myelinated) component providing rapid signals which control the heart and circulation, and consequently supporting the body to make rapid changes in movement.
- The physiological shift associated with changes in emotional state has been co-opted and subsequently adapted in mammals to facilitate social communication and group bonding.
- Human emotions have an additional level of complexity, thanks to a thinking capacity that allows us to use words to define our feelings, create thoughts and develop ideas. We relate to our internal thoughts as to any other aspect of our experience, by coding them with an emotional content.
- Love and other feelings may arise an emergent property of the autonomic nervous system, yet the meaning of what we experience is ours to choose, and our story to tell.
Text copyright © 2015 Mags Leighton. All rights reserved.
Acevedo, B. P et al. (2011). Neural correlates of long-term intense romantic love. Social Cognitive and Affective Neuroscience nsq092.
Alves, N.T. et al. (2008) Models of brain asymmetry in emotional processing. Psychology & Neuroscience 1, 63-66.
Arbib, M. A., & Fellous, J. M. (2004). Emotions: from brain to robot. Trends in Cognitive Sciences 8, 554-561.
Armour J A (1991) Anatomy and function of the intrathoracic neurons regulating the mammalian heart. In: Zucker, I. H., & Gilmore, J. P. (eds). Reflex control of the Circulation. CRC Press.
Armour, J. A. (2008). Potential clinical relevance of the ‘little brain’on the mammalian heart. Experimental Physiology, 93, 165-176.
Barrett, L.F. (2012) Emotions are real. Emotion 12, 413-429.
Bravo, J.A. et al. (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences, USA 108, 16050-16055.
Camp, B. J., & Norvell, M. J. (1966). The phenylethylamine alkaloids of native range plants. Economic Botany, 20, 274-278.
Carter, C.S. 2014) Oxytocin pathways and the evolution of human behaviour. Annual Review of Psychology 65, 17-39.
Fellous, J. M. (1999). Neuromodulatory basis of emotion. The Neuroscientist, 5, 283-294.
Fellous, J. M. (2004). From human emotions to robot emotions. In Architectures for Modeling Emotion: Cross-Disciplinary Foundations, American Association for Artificial Intelligence, 39-46.
Fisher, H. (2000) Lust, attraction, attachment: biology and evolution of the three primary emotion systems for mating, reproduction, and parenting Journal of Sex Education and Therapy 25; 96-104
Fisher, H. E. (1989). Evolution of human serial pairbonding. American Journal of Physical Anthropology 78, 331-354.
Fisher, H. E. (1998). Lust, attraction, and attachment in mammalian reproduction. Human Nature 9, 23-52.
Fisher, H. E. et al. (2002). Defining the brain systems of lust, romantic attraction, and attachment. Archives of sexual behavior 31, 413-419.
Fisher, H. E. et al. (2010). Reward, addiction, and emotion regulation systems associated with rejection in love. Journal of Neurophysiology, 104, 51-60.
Fisher, H. E., Aron, A., & Brown, L. L. (2006). Romantic love: a mammalian brain system for mate choice. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 361, 2173-2186.
Fitzgibbon, B.M. et al. (2014) The neural underpinnings of vicarious experience. Frontiers in Human Neuroscience 8, e384.
Genaro A. et al. (2014) Neurobiology of social attachments Neuroscience & Biobehavioral Reviews 43, 173–182
Gendron, M. et al. (2014) Perceptions of emotion from facial expressions are not culturally universal: evidence from a remote culture. Emotion 14, 251-262.
Gozal, E. A. et al. (2014). Anatomical and functional evidence for trace amines as unique modulators of locomotor function in the mammalian spinal cord. Frontiers in Neural Circuits 8, e134.
Greydanus, D.E. and Merrick, J. (2014) Newborn care: what we can learn from the kangaroo mother. Frontiers in Public Health 2, e96.
Herbert, C. et al. (2013) Your emotion or mine: labelling feelings alters emotional face perception – an ERP study on automatic and intentional affect labelling. Frontiers in Human Neuroscience 7, e378.
Insel, TR et al. (1995) Oxytocin and the molecular basis of monogamy. Advances in Experimental Medical Biology 395, 227-234.
Johnson, S. (2004) Mind Wide Open. Allen Lane; London
Kelly, A.M. and Goodson, J.L. (2014) Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches. Proceedings of the National Academy of Sciences of the United States of America 111, 6069–6074
Kelly, A.M. and Goodson, J.L. (2014) Social functions of individual vasopressin-oxytocin cell groups in vertebrates: what do we really know? Frontiers in Neuroendocrinology 35, 512-29
Kleinau, G. et al. (2011). Differential modulation of Beta-adrenergic receptor signaling by trace amine-associated receptor 1 agonists. PloS one, 6(10), e27073.
Lacey, B. C. & Lacey, J. I. (1978). Two-way communication between the heart and the brain: Significance of time within the cardiac cycle. American Psychologist 33, 99-113
Lambert, K.G. (2003) The life and career of Paul MacLean: a journey toward neurobiological and social harmony. Physiology & Behavior 79, 343-349.
Landete, J. M., Ferrer, S., & Pardo, I. (2007). Biogenic amine production by lactic acid bacteria, acetic bacteria and yeast isolated from wine. Food Control 18, 1569-1574.
Landete, J. M., Pardo, I., & Ferrer, S. (2007). Tyramine and phenylethylamine production among lactic acid bacteria isolated from wine. International Journal of Food Microbiology 115, 364-368.
Lieberwirth, C. and Wang, Z. (2014) Social bonding: regulation by neuropeptides. Frontiers in Neuroscience 24; 171.
Lindquist, K.A. (2013) Emotions emerge from more basic psychological ingredients: a modern psychological constructionist model. Emotion Review 5, 356-368.
Lindquist, K.A. and Gendron, M. (2013) What’s in a word? Language constructs emotion perception. Emotion Review 5, 66-71.
Lindquist, K.A. et al. (2012) The brain basis of emotion: a meta-analytic review. Behavioral and Brain Sciences 25, 121-202.
Lindquist, K.A. et al. (2014) Emotion perception, but not affect perception, is impaired with semantic memory loss. Emotion 14, 375-387.
Mallan, K. M. et al. (2013) Slithering snakes, angry men and out-group members: what and whom are we evolved to fear? Cognition and Emotion 27, 1168-1180.
Manini, B. et al. (2013) Mom feels what her child feels: thermal signatures of vicarious autonomic response while watching children in a stressful situation. Frontiers in Human Neuroscience 7, e299.
McCraty, R. (2002). Influence of cardiac afferent input on heart-brain synchronization and cognitive performance. International Journal of Psychophysiology 45, 72-73.
McCraty, R. & Childre, D. (2004). The Grateful Heart: the Psychophysiology of Appreciation. The Psychology of Gratitude Ch 12, 230-255.
McGraw, L.A. & Young, L.J. (2010). The prairie vole: an emerging model organism for understanding the social brain. Trends in Neurosciences 33, 103-109.
Niedenthal, P.M. et al. (1997) Being happy and seeing “happy”: emotional state mediates visual word recognition. Cognition and Emotion 11, 403-432.
Öhman, A. et al. (2012) Evolutionary derived modulations of attention to two common fear stimuli: serpents and hostile humans. Journal of Cognitive Psychology 24, 17-32.
Paterson, I. A. et al. (1990) 2‐Phenylethylamine: A Modulator of Catecholamine Transmission in the Mammalian Central Nervous System?. Journal of Neurochemistry 55, 1827-1837.
Pert, C. B. Molecules of emotion. 1997. New York: Scribner
Plutchik, R. (1980) Emotion: a psychoevolutionary synthesis. Harper and Row; New York.
Porges, S.W. (1997) Emotion: an evolutionary by-product of the neural regulation of the autonomic nervous system. Annals of the New York Academy of Sciences 807, 62-77.
Porges, S.W. (1998) Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 23, 837-861.
Porges, S.W. (2001) The polyvagal theory: phylogenetic substrates of a social nervous system. International Journal of Psychophysiology 42, 123-146.
Porges, S.W. (2003) The Polyvagal Theory: phylogenetic contributions to social behaviour. Physiology & Behavior 79, 503-513.
Porges, S.W. (2007) The polyvagal perspective. Biological Psychology 74, 116-143.
Rates, S.M.K. (2001). Plants as source of drugs. Toxicon 39, 603-613.
Reuter-Lorenz, P.A. et al. (1983) Hemispheric specialization and the perception of emotion: evidence from right-handers and from inverted and non-inverted left-handers. Neuropsychologia 21, 687-692.
Robles, T.F. and Kiecolt-Glaser, J.K. (2003) The physiology of marriage: pathways to health. Physiology & Behavior 79, 409-416.
Schneiderman I. et al. (2012) Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity Psychoneuroendocrinology 37, 1277–1285.
Schröder, T. and Thagard, P. (2013) Emotions as semantic pointers: constructive neural mechanisms. In The psychological construction of emotions (L.F. Barrett and J.A. Russell, eds). Guilford.
Schröder, T. and Thagard, P. (2014) Priming: constraint satisfaction and interactive competition. Social Cognition 32, 152-167.
Schröder, T. et al. (2014) Intention, emotion, and action: a neural theory based on semantic pointers. Cognitive Science 38, 851-880.
Schulkin, J. et al. (2003) Demythologizing and emotions: adaptation, cognition, and visceral representations of emotion in the nervous system. Brain and Cognition 52, 15-23.
Stock, S. and Uvnas-Moberg K. (1988) Increased plasma levels of oxytocin in response to afferent electrical stimulation of the sciatic and vagal nerves and in response to touch and pinch in anaesthetized rats. Acta Physiologica Scandinavica 132, 29-34.
Thagard, P. and Aubie, B. (2008) Emotional consciousness: a neural model of how cognitive appraisal and somatic perception interact to produce qualitative experience. Consciousness and Cognition 17, 811-834.
Wang, H. et al. (2013). Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nature neuroscience, 16, 919-924.
Yiend, J. (2010) The effects of emotion on attention: a review of attentional processing of emotional information. Cognition and Emotion 24, 3-47.
Zucchi, R. et al. (2006). Trace amine‐associated receptors and their ligands. British Journal of Pharmacology 149, 967-978.