Emotion and cortical-subcortical function: conceptual developments

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Abstract

Biologists have studied the expression of emotions in man and other animals since at least 1806, when Charles Bell published his Anatomy and Physiology of Expression. We trace the main experimental developments since that time, including Darwin's investigations into the evolution of innate forms of expression of emotions, as well as those into cognitive versus precognitive forms of expression of emotions. In particular, contemporary studies by neuroscientists into the origins of emotional experiences are detailed, especially emotional responses to faces showing different expressions, on which much research has been carried out. We examine the various claims made by these researchers as to what their experiments show. Our conceptual analysis indicates that there is considerable confusion as to what experimental work to this time indicates about the role of cortical and subcortical structures in the expression of emotions. We attempt to clarify what can and cannot be justified as established concerning the workings of the brain and emotions.

Introduction

Fruitful research on the emotions requires clarity with regard to the category of the emotions and the differentiation of emotions from feelings that are not emotions at all, although commonly confused with them. So before recounting some of the salient advances in research over the past century or so, we shall endeavour to provide a schematic map of the conceptual terrain.

Feelings must be differentiated into sensations, tactile perceptions, appetites, and affections (see Fig. 1 as well as Bennett and Hacker (2003, Chapter 7). Pains, tickles and tingles are bodily sensations with a more or less determinate bodily location. They are felt in a part of the body, but not with a part of the body. Unlike perceptions, sensations are not correct or incorrect, and are not susceptible to cognitive error. There is no such thing as thinking one is in pain but being mistaken. Phantom pains or reflected pains may lead one to judge that one has an injury where there is none, but what is erroneous is neither the sensation nor its felt location – it is the judgement concerning the location of the injury. Localised bodily sensations must be distinguished from sensations of overall bodily condition, such as feelings of weariness or lassitude. Feeling the heat, solidity, elasticity or dampness of an object are forms of tactile perception – exercises of a cognitive faculty that inform one how things are in one's environment in respect of perceptible qualities such as warmth, cold, hardness, softness, wetness, dryness, and so forth. Like all perceptions, they may be correct or incorrect, and we distinguish between things feeling thus and so to one, and things being thus and so. Natural appetites are such things as feelings of hunger, thirst or animal lust. Non-natural (acquired) appetites are addictions.

An appetite is a blend of desire and sensation. Sensations characteristic of appetites have a bodily location (sensations of hunger are located in one's midriff) and are forms of unease that dispose one to action to satisfy the desire. The desire that is blended with sensation is characterised by its formal object: hunger is a desire for food, thirst for drink, lust for sexual intercourse. The intensity of the desire is typically proportional to the intensity of the sensation. Fulfilling an appetite leads to its temporary satiation and so to the disappearance of the sensation. Appetites are not constant, but recurrent, typically caused by bodily needs or hormonally determined drives.

Affections too are felt. The feelings that are affections can be distinguished into agitations (e.g. astonishment, excitement), moods (e.g. cheerfulness, depression) and emotions (e.g. fear, love) – see Fig. 2. Unlike sensations, affections do not inform one about the state of one's body, though they are sometimes linked with sensations. One does not feel pride in one's chest, even though one's chest may swell with pride, or fear in one's mouth, even though one's mouth may be dry with fear. One's blush of embarrassment does not inform one of the state of one's facial arteries, although it may inform one that one is more embarrassed than one thought, and one's tears of grief do not inform one of the state of one's lachrymal glands, although they may inform one that one is grieving more than one anticipated. Unlike feelings that are perceptions, the affections do not inform one of the state of the world around one. Paradigmatic emotions are love, hate, hope, fear, anger, gratitude, resentment, indignation, envy, jealousy, pity, compassion, grief, as well as emotions of self-assessment such as pride, shame, humiliation, regret, remorse and guilt.

Agitations are short-term affective disturbances, commonly (but not only) caused by something unexpected, e.g. being and feeling excited, thrilled, shocked, convulsed, amazed, surprised, horrified, disgusted, delighted. They are caused by what we perceive, learn or realise. Because they are disturbances, caused by unanticipated disruptions, they are not motives for action as emotions may be, but temporarily inhibit motivated action. One's agitations are manifested in expressive behaviour because one is, for example, excited, surprised, or shocked, but one does not act out of excitement, surprise or shock as one may act out of love, pity or gratitude. Agitations are modes of reaction: one cries out in horror, recoils with revulsion, is convulsed by laughter, or is paralysed with shock. Occurrently felt emotions, as opposed to longer standing emotional attitudes, often bear a kinship to agitations, for example in the perturbations of rage, fear and grief.

Moods are such things as feeling cheerful, euphoric, contented, irritable, melancholic or depressed. They are states or frames of mind. They may be occurrent, or longer-term dispositional states (one may feel depressed for an afternoon, or one may be suffering from a depression that lasts for months – being then prone to feel depressed during one's waking hours). Moods are less closely tied to specific objects than emotions – one can feel cheerful without feeling cheerful about anything in particular, but one cannot love without loving someone or something in particular. They are not linked to specific patterns of intentional action, since, unlike emotions, they do not afford motives for action. Moods colour one's thoughts and pervade one's reflections. So they are linked to manners of behaviour, demeanour and tone of voice.

It is important, especially in the study of human emotions, to distinguish between episodic emotional perturbations and emotional attitudes. Emotional perturbations resemble agitations in certain respects. Some, e.g. fear or anger, have characteristic somatic accompaniments, both sensations that are felt and physiological reactions that are measurable. Others do not, e.g. feelings of pride, humility, compassion, and gratitude. They are manifest in expressive behaviour that may take various forms. It may be behaviour that is not action, such as blushes, perspiration, pallor. It may be voluntary (utterances of love and affection, hope or pride), partly voluntary (raised voice of anger, that can be suppressed) or involuntary action (cry of terror). It may be exhibited only in the manner of acting (e.g. tone of voice, impatient gestures).

Emotional attitudes, such as love, hate, pride, shame, remorse may last for long periods of time and motivate action done for reasons. One may love or hate a person, activity, a cause or place for years. One may be proud of the achievements of one's youth for the rest of one's life, and one may respect or detest, be jealous or envious of someone for years. One may be ashamed or guilty of one's misconduct for decades, and one's regrets for one's follies may never cease. One's judgement may be clouded not only by emotional perturbations but also by one's long-standing resentments, envies or jealousies. The emotions of love, hate or envy, for example, consist above all in the manner in which the object of one's emotion matters to one and the reasons one has for holding it to be important, and hence too in the motives it affords one for acting (for one acts out of love, hate or envy). One's emotions are then evident in the reasons that weigh with one in one's deliberations, in the desires one harbours in respect of the object of the emotion, and in associated thoughts and fantasies.

Emotions have objects as well as causes. What makes one afraid (a noise downstairs at night) need not be what one is afraid of (a burglar, who may not even exist). What one is frightened by is the cause of one's fear, what one is frightened of is its object. What makes one feel ashamed, e.g. someone's indignant tirade, is not the same as what one is ashamed of, namely one's own misdemeanour. A person need not know the cause of his emotion, but, save in pathological cases, he cannot be ignorant of the object of his emotion, i.e. whom he is angry with, what he is ashamed of, what he is afraid of.

It is obvious that the intensity of one's emotions is not proportional to the intensity of whatever sensations may accompany their occurrent manifestations. One's pride in one's children's achievements cannot be measured somatically, but may be manifest in one's behaviour, in the way one praises them and how one talks about them. One's fear of heights may be manifest above all in the lengths one goes to avoid them, rather than in any perturbations – given that one avoids heights at all costs. Unlike appetites, emotions do not display the same pattern of occurrence, satiation, and recurrence. They have a cognitive dimension absent from appetites. For the frightened animal is afraid of something it knows or believes to be dangerous or harmful, a mother is proud of her offspring, believing them to be meritorious, and the repentant offender is remorseful, knowing or believing himself to have done wrong and wishing to make amends. Human emotions, rooted though they are in our animal nature, are nevertheless run through, as mere animal emotions are not, with thought and belief, wish and want, fantasy and imagination – as should be expected of language-using, concept-exercising creatures.

Section snippets

Darwin

In 1872, Charles Darwin published his book The Expression of Emotions in Man and Animals (Darwin, 1965). The scope of the book was wider than suggested by the title, since Darwin investigated expressive behaviour in general, studying not only the expressions of fear, anger, grief, etc., but also behaviour expressing pain, assent, dissent, puzzlement, and helplessness, which are not emotions. Expressive behaviour can be differentiated into facial expression, movements of the body and limbs,

Cognitive versus precognitive theories for the expression of emotions

Scientists have differed over the relation between emotion and cognition. Zajonc (1984) has been a main proponent of the view that ‘affect and cognition are separate and partially independent systems and although they ordinarily function conjointly, affect could be generated without a prior cognitive process.’ Thus, according to Zajonc, affective judgements may be made on first meeting a person even though very little of what he refers to as ‘cognitive processing’ has taken place. Evidence

Faces expressing different emotions and the amygdala: PET and fMRI

There is direct in vivo evidence for a differential neural response in the human amygdala that accompanies facial expressions of fear and happiness (Morris et al., 1996). Positron-emission tomography (PET) measures of neural activity were acquired while subjects viewed photographs of fearful or happy faces, varying systematically in emotional intensity. This work showed that the neuronal response in the left amygdala is significantly greater when viewing fearful photographs as opposed to those

Behavioural studies involving face recognition following damage to the orbitofrontal cortex

As noted above, damage to the orbitofrontal cortex in primates leads to reduced aggression to sighted objects that would normally produce fear, such as a human being or a snake (Butter and Snyder, 1972). Furthermore, neurons that fire maximally when the animal sees a face are found in the orbitofrontal cortex, as shown in Fig. 12. This figure shows the firing rate of impulses for the neuron recorded from the orbitofrontal cortex in the left hand column when the macaque monkey was presented with

Neural networks: amygdala and orbitofrontal cortex in vision

In this section we shall consider the networks of connections of the amygdala and orbitofrontal cortex. In the overview of these networks provided in Fig. 15, connections are shown to the amygdala and the orbitofrontal cortex from the ventral visual stream including V1 to V2, V4 and the inferior temporal visual cortex as well as connections from the primary taste and olfactory cortices. In addition, connections are shown from the somatosensory cortical areas 1, 2 and 3 that reach the

The claims of LeDoux

The concept of ‘working memory’ plays an important part in LeDoux's ideas on the relation between activity in the brain and emotional experience. Goldman-Rakic and her colleagues argue that the neural networks involved in working memory support the capacity to hold an item of information for several seconds so that it may be utilised for the temporal integration of present sensory stimuli with those involving a memory of recent past occasions. Such networks in prefrontal cortex possess neurons

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