Fear and Loathing in the Human Brain
by Dr Andy Calder
Research addressing the brain regions involved in human emotion has expanded rapidly in recent years. This is, in part, due to the widening availability of new brain imaging technology, but also to a newfound interest in the idea that certain individual emotions may be served by separate brain systems. This latter theoretical position is at the heart of the idea that selected sets of so-called "basic" emotions with strong evolutionary histories constitute the foundations of human emotion.
Although this concept has its origins in the work of Charles Darwin, it only really took off following the work of psychologists such as Silvan Tomkins, Paul Ekman, and Carol Izard in the 1960s and 70s. Prior to this, emotion research was dominated by the idea that all emotions were coded as values on a limited number of dimensions or scales coding more general emotional constructs, such as valence (how positive or negative an emotion is) and arousal (whether the emotion is associated with low arousal or high arousal).
Similarly, early neurological accounts of emotion processing took a similar all-encompassing approach in which all emotions were processed by a circuit of interconnected brain structures known as the limbic system.
Two important findings of Ekman and his contemporaries that changed theories of emotion were studies demonstrating that certain emotions (happiness, sadness, anger, fear, and disgust) were associated with distinct facial signals, and that these were common to cultures throughout the world; observations that now constitute two of the defining features of basic emotions.
A third posited feature was the idea that each basic emotion should be associated with a distinct (neuro)physiological signature, such as a particular brain circuit or a more peripheral body state response, including heart rate, or galvanic skin response (an index of lying in the famous lie detector test) and so on. Human evidence consistent with this third feature proved difficult to find; However, support was found in non-human biological studies by researchers such as Joe LeDoux and Jaak Panksepp.
It is of considerable interest, then, that work with humans over the last eight years has begun to identify that certain emotions may be coded by partially distinct brain systems as Ekman and his colleagues had predicted. This research has been aided greatly by recent advances in brain imaging technology that allows more precise localisation of the regions damaged in brain-injured patients, and identification of the areas of the brain that are activated in healthy individuals when they perform a psychological task. A large number of these studies have addressed the areas of our brain that are used to recognise emotion in others; in other words brain systems involved in recognising facial and vocal signals of emotion. Two emotions that have received considerable amount of attention are fear and disgust.
To date brain imaging technology and work with patients who have suffered brain injuries has shown that a small almond-shaped structure in the brain called the amygdala, plays a significant role in recognising facial and vocal expressions of fear. For example, my colleagues and I at Cambridge University studied a lady known as DR who underwent neurosurgery to relieve epilepsy that was resistant to pharmacological treatment. The cause of DR's epilepsy was her left and right amygdala, and the surgeon removed both structures in an attempt to reduce the frequency of her epileptic fits. Calder and colleagues demonstrated that DR showed an impaired ability to recognise fear, and to a lesser extent anger from facial and vocal expressions of emotion, whereas her recognition of other emotional expressions was normal. This showed that amygdala was important for recognising these emotions.
In related work, researchers such as Antoine Bechara in Iowa and Kevin LaBar at Duke University have shown that the amygdala is also important in acquiring new fear reactions towards previously harmless objects via a procedure know as fear conditioning. This is normally demonstrated by simultaneously presenting an individual with a "neutral" object, such as a cup, together with a mild electronic shock, or startlingly loud noise. As a result, the individual acquires a mild fear towards the previously neutral cup that can be detected as increased galvanic skin response when the cup is presented alone. A similar mechanism is thought to underlie the acquisition of common phobias, such as fear of spiders. Bechara and LaBar showed that individuals with amygdala damage do not show fear conditioning, and concluded that this region plays a central role in this psychological function.
An obvious question was whether emotions other than fear might be associated with relatively specialised brain systems, and there is now good evidence that a brain region known as the insula underlies the recognition of human signals of disgust.
Support for this position comes from both brain imaging research and neuropsychological studies of brain-injured patients. A particularly striking example comes from work by my colleagues and I. These researchers studied the performance of a young male with insula damage, known as NK. In a series of experiments they showed that NK demonstrates a highly selective impairment in recognising disgust from facial and vocal signals. In comparison to healthy volunteers with no brain injury, NK also demonstrates a marked reduction in his reactions to disgusting items. For example, in a questionnaire measuring how sensitive an individual is to different disgust-provoking situations, healthy control subjects consistently respond "no" to the question "If you were hungry would you eat a bowl of soup that had been stirred with a washed fly swatter". By contrast, NK was adamant that he would have no difficulty in consuming the soup.
Research on disgust has also been advanced by the work of Pierre Krolak-Salmon and colleagues in Lyon who have studied the electrical activity in the brain in response to viewing pictures of different facial expressions. The subjects in this study were patients waiting to undergo surgery for epilepsy. To investigate the brain regions causing the epilepsy the patients had electrodes implanted in different brain regions, including the insula. Krolak-Salmon and colleagues were able to show that electrodes in a particular area of insular cortex showed a strong response to facial expressions of disgust, but not to expressions of other emotions. Moreover, stimulation of the electrodes caused unpleasant sensations in the throat spreading to the mouth, lips and nose – an effect reminiscent of nausea reactions reported by Wilder Penfield in a famous study investigating electrical stimulation of the insula in neurological patients reported some 50 years previous.
On the basis of these findings I and my colleagues have argued that the human brain contains partially separate, but interconnected neural systems coding fear and disgust. In addition, they suggest that both systems pass information on to a further emotion system located in frontal lobes of the brain. The idea that these systems are interconnected and talk to one another is essential, because many of the emotional situations we encounter in everyday life contain a blend of emotions. For example, some situations are both disgusting and frightening, and many Hollywood films including Seven and Silence of the Lambs capitalise on this for maximal emotional effect.
An important question is why emotions such as fear and disgust should be associated with relatively specialised neural machinery, do these emotions have some kind of special status? The answer to this question may well be yes because both play central roles in ensuring that an individual avoids dangerous or harmful situations and substances. In the case of fear, that danger may be from a predator or more dominant member of the same species, whereas for disgust the danger may be related to the potentially contaminating effects of rotten food or stagnant water, for example.
While many further issues in this area remain to be addressed, I hope it is nonetheless clear that research into the manner in which the human mind processes emotion and emotional signals is an exciting and fascinating component of research in human cognitive neuroscience.