Review
The diverse neurogeography of emotional experience: Form follows function

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Abstract

The experience of emotion underlies emotional expression and consequent action. Although several theoretical models of emotion have suggested that emotional expression is reciprocally involved with sensory inputs and behavioural responses to environmental stimuli, these discussions have largely focused upon fear and its survival value to the organism. By describing research studies across a wide range of emotions and the specific brain regions that are associated with those emotions, this review raises the hypothesis that the “form” of emotional experience neurogeography has followed the “function” associated with developing complex emotional and behavioural responses to challenging environmental stimuli. This separation of emotions within the brain thus confers a survival advantage for the organism in terms of reproduction, safety, and development of more effective problem-solving strategies.

Research highlights

▶ Emotional experience is dispersed across brain regions (tabulated). ▶ This dispersal allows simultaneous experience of different emotions. ▶ Resultant behavioural plasticity may provide an evolutionary advantage.

Introduction

Emotion has been described as having three major components [1]: emotional behaviour (changes in physiology induced by the autonomic nervous system), emotional communication (words, facial expressions, gestures), and emotional experience or feelings. However, the neurological experience of emotion logically precedes its expression in internal physiological behaviour or communication, and may be defined as those synaptic processes which are associated with emotional experiences, and which may instigate physiological responses commonly ascribed to emotion. This discussion will focus upon emotional experience, and includes any of the three primary emotions (anger, fear, joy: [2], [3], plus those secondary emotions which may include guilt, sadness, melancholy, embarrassment, regret, as well as several others [2].

Various physiological theories of the purpose of emotion have been proposed (e.g. [4], [5], [6], most of which focus on the link between emotions and physiological change, such as smiling may cause the emotional experience of happiness [7], [8]. However, these simple one-way models of emotion-causing-physiology or vice –versa have been shown to be of limited value in explaining other emotions. There are also several psychological theories of emotion and its function [9], [10], [11], [12] but these do not deal directly with the neurobiological substrates of the experience of emotion. Instead, it is worthwhile to reflect upon the hypothesis that emotion (like most behaviour that is common across cultures and transmitted between generations) has been selected by evolutionary processes. Therefore, emotion may be accepted as a particular kind of neurological-behavioural phenomenon, which exists because it confers a reproductive advantage upon the organism experiencing the emotion. Dobzhansky's comment that “…nothing makes sense in biology except in the light of evolution” [13, p. 449] reiterates Darwin's argument that emotion evolved because it functions to help the individual preserve self by assisting it to make survival responses to environmental demands [14]. Working from this perspective, unidirectional models of emotion (as described above) have been replaced by more recent and detailed descriptions that incorporate sensory input, synaptic activity and physiological responses as reciprocating steps along the pathway to and from emotional experience, at least in regard to the emotion of fear [15].

LeDoux's [16] hypothetical explanation of the function of fear is that sensory information about a threatening stimulus is processed first by the thalamus and then the amygdala, which initiates fast and influential neurological reactions that are experienced by the individual as “fear” and which instigate physiological responses (via the hypothalamus and the sympathetic nervous system) that have been highly selected for survival value by their evolutionary consequences. LeDoux's argument is based upon the evolutionary success of fast fear responses in terms of individual and group survival and, as such, is convincing (even if not original –Darwin suggested the same hypothesis in 1872), but it does not immediately generalize to other primary emotions such as anger and joy, plus secondary emotions mentioned above which do not have such immediately apparent survival value.

That is, when applied to fear, and also to the other two primary emotions (joy, anger), the immediate self-preserving benefits of these emotions are possible to determine. For example, anger may facilitate temporary increases in physical strength [17] and thus may have some selective advantage when the organism is confronted by competitors. Joy, like the secondary emotions, may have its original value as a communication strategy in social situations, with generalization to individual (i.e. private) experience via associative conditioning. While this joy-based linking with others may enhance group solidarity (and survival), many secondary emotions are not shared in this way and their reproductive advantage is less easily demonstrated, despite the frequency and intensity of their experience by individuals.

However, even if all emotions are shown to have survival value, the experience of emotion is only a stage in the overall process of instigating behaviour that assists the individual or the group to pass on the gene pool. That is, the experience of emotion has been conceptualized as not holding survival value for the individual experiencing it apart from its role as an instigator of behaviour, because it is the overt behaviour that arises from emotion, which confers any survival value to the individual. Therefore, the experience of emotion, although being a vital stage in the processing of sensory information and consequent behavioural response (which enhances survival) must be managed by the brain in ways that do not interfere with other “background” brain-controlled activities (such as breathing, digestion, maintenance of temperature, etc) or the immediate and powerful physiological responses to emotional experience which enable the organism to escape threat, defend territory or build social cohesion with peers. In addition, the experience of emotion may also function as an aid to comprehension of environmental events. In that case, more complex emotional responses may have higher potential value because they encompass more of the detail in the environmental event. Enabling the full complexity of emotional responses to be experienced may rely upon particular brain architecture which may, in turn, be selected and genetically transmitted to offspring because of its survival value.

One possible strategy to enable the brain to produce emotional experiences while maintaining the body and instigating rapid behaviour changes, and also to enable the organism to experience a range of emotions to complex environmental events, may be to separate emotional experiences into different brain regions. In doing so, this may enable major neural substrates and circuits to be specifically devoted to particular emotions and also to share the neurological demand across those regions, thus maximizing the outcomes available to the individual in terms of survival benefits. Although only an hypothesis at this stage, this assumption is not without some logic when compared to other brain functions that also integrate different brain areas into cohesive actions which facilitate survival responses by the organism (e.g. processing of visual stimuli, or the actions of the reticular systems). Data which support this hypothesis of “space-sharing” in brain region experience of emotion are found in studies of the neurogeography of emotion, and will be reviewed below to explore this hypothesis.

Section snippets

Bilateralisation of emotional experiences

A great deal has been written regarding the hypothesis that the right hand side of the brain is more likely to show emotional activity than the left hand side [18], [19]. While this may be more likely to be associated with highly-arousing unpleasant emotions such as fear and anger [20], 1999), a more recent review noted that there was no significant difference between left- and right-handed activations over a range of positive and negative emotions [21]. Additionally, although there are some

Reviews

As well as the original studies examined above, several major reviews also cast light upon the issue of brain region activity during emotional experience. Phan et al. [60] performed a meta-analysis of 43 PET and 12 fMRI studies of emotion in healthy subjects that evaluated brain region activity for the emotions of sadness, fear, disgust and happiness which were presented either via visual or auditory stimuli, or self-reflection of a time when the subjects felt a particular emotion. A total of

Discussion

Table 1 presents a tabulation of the various brain regions that have been associated with specific emotions, and supports the hypothesis that the complexity and interrelatedness of the brain's regional processing of emotion strongly argues against a single emotion-responsible region or group of regions. Although the limbic system has been described for some time as the emotion centre of the brain, these data challenge the completeness of that description. Clearly, multiple brain sites are

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