It is now widely recognized that a purely cognitive approach to mental function that ignores emotions is at best incomplete. And the limbic system theory of emotion no longer carries the explanatory weight it once did. With these hindrances now in the background, emotions are being avidly pursued across the spectrum of neuroscience, occupying the interests of researchers who study genes and their molecular products, cellular physiological properties of neurons in dishes as well as in living brains, pharmacology of synaptic transmission, behavioural processes, computer simulations of brain function, and imaging of normal subjects and neurological and psychiatric patients. Emotions, in short, are hot.
1. The credibility problem
2. Emotions, one at a time
3. Defence
4. Conscious feelings
5. The future of the brain
1. The credibility problem
As with any other psychological process, the pursuit of emotions in the brain is only as good as our understanding of the process itself. In order for interest in emotions to be sustained, it is thus important that we develop rigorous ways of thinking about the underlying processes in a way that will make it possible to relate specific aspects of emotion to detailed brain mechanisms. Fortunately, such an approach has recently begun to emerge.In the late 19th century, William James and other psychologists came to think of emotions as having two components: a subjective or conscious manifestation, typically referred to as an emotional feeling, and a set of behavioural and physiological body alterations called emotional responses. Following this lead, researchers interested in the brain mechanisms of emotion often proposed different systems for conscious feelings and emotional responses.
Problems quickly arose. The partition between the conscious and bodily components of emotion was nothing more than a scientific restatement of the philosophical mind–body problem in the realm of emotion. And to make matters worse, most brain research was, and still is, conducted in non-human species, organisms in which there is little scientific evidence (as opposed to anecdotal stories and hard-felt beliefs) for the existence of subjective conscious states. In spite of this, most theorists discussing the brain mechanisms of emotion — from James to Cannon to Papez and MacLean, to name some of the key historical figures — used this research on non-human organisms to generate theories of how emotional experiences are mediated by the brain. This has created a credibility gap between the research itself and its application, a gap that must be overcome in order for emotion research to progress.
We readily make the leap about consciousness from our own mind to minds of other humans — life as we know it would be impossible otherwise. So why shouldn't we do the same for other animals? All we really have on which to base our conclusion about mental states in either case is overt behaviour. If another person or another animal acts the same as we do, shouldn't we assume they have the same internal states? Other humans, yes; other creatures, no. All humans have pretty much the same kind of brain, but there are important differences between the brains of humans and other animals, including other primates. And the parts of the brain that are most different (the prefrontal areas) are just the ones that are key to higher mental processes, and possibly to consciousness. This anatomical fact alone forces us to be extremely cautious in drawing conclusions about an animal's mental states on the basis of the similarity of its behaviour to ours. A cockroach runs away under the shadow of a descending human foot, just as we run if we notice something falling towards us. But it is unlikely that the roach feels the fear that a human does when doing essentially the same thing under similar circumstances. So where do we draw the line as to conclusions about whether different organisms have different mental states? Vertebrates vs. invertebrates? Reptiles vs. mammals? Primates vs. other mammals? I would say that the safest conclusion on scientific grounds is to assume that organisms with similar brains (same neural systems) have similar kinds of mental states, and organisms with brains that have verifiably different neural systems are likely to have different kinds of mental states. This does not mean that a monkey, cat, dog, rat, frog, lizard, or pigeon has no feelings. It means that if they do have feelings the feelings they have are likely to be different from the ones we have since our brains differ from theirs.
In all fairness, researchers in other areas of psychology were, for quite some time, really no better off than emotion researchers when it came to relating mental states to brain mechanisms. There is nothing less subjective about a conscious perception or a conscious memory than a conscious emotion. But a way emerged for closing the credibility gap for cognitive processes like perception and memory. With the rise of cognitive science came a way of studying how the brain systems process information independent of whether, and if so how, that information enters conscious awareness. For example, much has been learned about how the brain processes colour while little is still known about how the brain experiences colour. Presumably, the mechanisms that process colour are involved in the experience of colour, but the experience of colour is the end result rather than primary subject of interest. One important consequence of this view is the conclusion that we are not conscious of the processing that leads to an experience — information processing is by default unconscious. This point was made by Karl Lashley many years ago but has since become a cornerstone of the cognitive approach to the mind.
Emotion, though, was not part of the cognitive revolution in psychology and the processing approach was not applied to this topic. But there is no real reason why emotion cannot, like cognition, be thought of in terms of processing functions. Indeed, in recent years, the processing logic can and has been fruitfully applied to the study of emotion, thus overcoming the credibility problem. That is, it is possible to study how the brain of a human or other animal detects and responds to danger, food, sexual partners, and so forth without first understanding how we consciously experience fear, gustatory delight, or sexual pleasure. The relevant stimuli, in other words, are processed unconsciously, and on the basis of this processing appropriate responses are initiated and controlled. This point of view offers a great advantage in the study of other creatures. Given that animal research is key to understanding brain mechanisms at a detailed level, and that we cannot inspect the inside of an animal's mind, the ability to close the credibility gap is not only useful, it is essential to progress in understanding the emotional brain.
2. Emotions, one at a time
In providing a way of thinking of emotions as processing functions of the brain, the processing logic gave a great boost to modern studies of the emotional brain. But there was another important development. In the past, researchers treated 'emotion' as a brain function. The limbic system, for example, was said to be the seat of 'emotion', in the general sense of the term. But in trying to be everything to all emotions, the limbic system theory failed to provide an adequate explanation of how any particular emotion process is represented in the brain. This convinced many researchers to turn to a different approach, one that assumes that there are different systems in the brain for different emotions.This approach would seem to overlap considerably with the psychological notion of 'basic emotions', which assumes the existence of a set of biologically determined primary emotions, such as fear, anger, joy, disgust, and so forth. However, the brain approach is fundamentally different. The psychological basic emotions are defined on the basis of human subjective experience, and thus take us back to consciousness and the credibility problem. The brain science approach, in contrast, starts with an animal behaviour system, like the defence system, and tries to understand how this system detects and responds to danger. For convenience, the defence system is often called the fear system. But when this is done, it is with the understanding that fear responses, not fearful experiences, are the topic of investigation. This understandably sometimes leads to confusion outside the field.
3. Defence
The defence system is the most extensively studied emotion system of the brain. While there are a number of different approaches to studying defensive behaviour, much of our current understanding comes from studies of a particular behavioural paradigm called classical fear (or defensive) conditioning. This is a variant on Pavlovian conditioning in which an aversive stimulus, such as an electric shock, occurs in association with an emotionally neutral stimulus, such as pure tone. After only a few pairings (one is enough) a long-lasting memory of the experience is established such that the next time the subject encounters the tone it will express defence responses — freezing behaviour, changes in blood pressure and heart rate, stress hormone release, and so on. The sound serves as a warning signal that danger may be imminent, and bodily resources are mobilized to deal with the impending threat.The neural system underlying this form of emotional learning is well characterized in studies of rats. It involves the transmission of sensory information to the amygdala, and the control of defence responses by way of output connections of the amygdala (see emotion). Within the amygdala two nuclei are especially important — the lateral (input region) and central (output region). Connections between these allow the stimulus to elicit the responses after the sound has been paired with the shock. Neurons in the lateral nucleus receive information about the sound and the shock and appear to be crucially involved in the learning process. Recent studies on a number of different fronts have begun to pinpoint the exact cellular and molecular changes that underlie the learning, implicating specific neurotransmitters and specific intracellular pathways leading to gene induction and protein synthesis.
One interesting feature of the defence system is that it can be activated by information from either the thalamus or the cortex. Given that the cortex is likely to be involved in the conscious awareness of the stimulus, in the case of thalamic activation, the amygdala can begin to respond before we 'know' what we are responding to. This has implications for understanding psychiatric conditions characterized by uncontrolled and unexplained fear — perhaps the amygdala is being rapidly triggered by stimulus elements that are processed differently at the cortical level.
Recent studies of patients with amygdala lesions, or damage to the temporal lobe that includes the amygdala, have verified that this region is also necessary for defence conditioning in people. Further, functional imaging studies have shown that the amygdala is activated during defence conditioning. Interestingly, one study found evidence for thalamic as opposed to cortical activation of the human amygdala, confirming the rat work.
4. Conscious feelings
There is a growing consensus in cognitive neuroscience that consciousness in humans critically depends on working memory functions distributed across several regions of the prefrontal cortex. This notion is readily extended to account for emotional feelings. When an emotion-unconscious processing system, like the defence system involving the amygdala, is activated, it calls into play a variety of other brain systems, including memory systems that function implicitly (unconsciously) and explicitly (consciously accessible), arousal systems in the brain stem that activate forebrain regions, and bodily responses that feed back to the brain. When the activity of these various systems is represented in working memory, conscious states become conscious emotional states, that is, emotional feelings. Because of the widespread and diverse activation of brain and body systems during emotional states, the experience tends to be more intense and longer lasting. Intensity and duration, in fact, distinguish emotional from non-emotional experiences. An alternative view of conscious emotional feelings is that they are defined by bodily states. This view, which overlaps considerably with William James's theory, mainly differs from the working memory view in emphasis.5. The future of the brain
While considerable progress has been made in understanding the emotional brain, much work remains. In particular, future work needs to account more thoroughly for the organization of fear in the brain and to explore other emotions in comparable detail. In addition, the manner in which emotional and non-emotional, especially cognitive, systems, interact needs to be unravelled. This will allow research on the brain to move beyond an emphasis on either cognition or emotion and towards broader questions, especially questions about how the brain creates the self, which is neither cognitive nor emotional, but both, and more.(Published 2004)
— Joseph LeDoux
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