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Parallel Memories: Putting Emotions Back Into The Brain
A Talk With Joseph LeDoux

JB: Emotions and the brain? Isn't this something new for scientists?

LEDOUX: Twenty years ago no one cared about emotions and the brain, but it seems in the last couple of years there's been a flurry of activity. One reason for this may be that the topic was ignored for so long, and the vacuum is being filled. Another, though, is that there have been some successes in approaching the problem, and these have changed peoples' minds about the feasibility of studying emotions in the brain.

The most successful efforts have come from the study of fear. Fear is a relatively tractable emotion, unlike love or hope which are difficult to pin down. It's always easier to study brain functions that involve clearly defined stimuli and responses than those that don't. For fear, you can easily create experimental situations where the onset of a simple stimulus that warns of impending danger elicits a set of stereotyped responses in an animal, like a rat, that are very similar to the kinds of responses that occur in a human facing danger. By following the flow of the stimulus through the brain from the stimulus processing pathways to the response control networks, it's possible to identify the basic neural circuits involved. We've done this for fear.

JB: How did you get into this?

LEDOUX: I got interested in emotions while I was studying something completely different. I was doing split-brain research as a graduate student with Mike Gazzaniga. Mike and I were studying how information is transferred between the hemispheres of these patients. One of the questions we asked was what happens when we put information in the right hemisphere. Remember, it's the left hemisphere that usually does the talking, so information in the right hemisphere can't ordinarily be talked about in these patients. We put emotional information in the right hemisphere, and the left hemisphere couldn't tell us what it saw, but it could tell us how it felt about it. That led us to the idea that emotional information and information about the content of what a stimulus is, are processed by different pathways in the brain. That seemed very interesting, and I decided I wanted to pursue it.

At the time, I felt that the only way to go about studies of the pathways of emotional processing was to turn to an animal model, where you can do experimental lesions, cell recordings, pathway tracing and so on. The reason you want to do these kinds of studies is not to satisfy some reductionistic urge, but because they can help you see how emotion is put together in the brain, and this can tell you about how the function itself works. Today, there are more sophisticated ways of studying the human brain, such as functional imaging. These can give you a picture of the brain in some emotional state, but you can't then ask the next question. You want to know how the activated region fits into a larger system. You really can't get to those kinds of questions in humans and have to turn to the animal models for answers. The animal work, in other words, gives the framework for interpreting the snapshots we get from human imaging studies. Without the animal studies, though, many of the human studies probably never have been done, and if they had, they wouldn't be so readily interpretable.

So I left the world of human neuropsychology and went into animal research after finishing my PhD and a short post doc. Mike and I had moved to Cornell Medical School and after a year or so I hooked up with Don Reis in the Neurobiology Lab there. The lab's mission was to study the brain's control over the autonomic nervous system, and basically I was told that I could do whatever I wanted as long as I recorded blood pressure. So I developed a blood pressure model of conditioned fear.

I used conditioned fear because it seemed like a relatively straightforward technique: you give a meaningless tone followed by a mild shock a few times, and pretty soon the tone starts eliciting a blood pressure response. It was a good way to create an emotional reaction to the tone on the spot in an animal that wasn't afraid of the tone and didn't have any emotional reaction to it to begin with. Since the tone gets to the brain by way of the auditory system and the response comes out of the brain through the autonomic nervous system, the trick was to figure out how the auditory system is linked up with the autonomic system. By using a combination of brain lesions, neural recordings, and pathway tracing techniques, we were able to figure this out. The answer, in short, is that the amygdala turned out to be a necessary and sufficient link between the auditory system and the autonomic nervous system. However, in a more general sense, the amygdala is the link between all sensory systems and all fear responses systems. It's the part of the brain involved independent of how the stimulus gets into the brain and how the response comes out.

JB: I find it interesting that the first emotion you studied was fear.

LEDOUX: When I first began this work in the early 1980s, I was using fear conditioning techniques because they were convenient. As I said, you can take the stimulus, pair it with the shock one or two times and, as a result, create an emotional reaction that's relatively profound in the animal. I thought at the time that this was going to be a way of identifying a universal emotional system in the brain, something akin to the limbic system. I no longer feel that way. I think that the study of the limbic system, or more generally the idea that there is an emotion system in the brain, is misguided. I came to this conclusion empirically. Once we had outlined a neural circuit for fear responses, it was obvious that the limbic system had little to do with it. The only so-called limbic area involved was the amygdala. And the hippocampus, the centerpiece of the limbic system, had been implicated in non-emotional processes like memory and spatial behavior. It seemed clear that the limbic system, if it existed at all, was not systematically involved in any clear way. I decided I didn't need the limbic system concept to think about how fear works in the brain. But that still doesn't wholly justify the focus on fear to the exclusion of other emotions.

I've come to think that emotions are products of different systems, each of which evolved to take care of problems of survival, like defending against danger, finding mates and food, and so forth. These systems solve behavioral problems of survival. Detecting and responding to danger requires different kinds of sensory and cognitive processes, and different kinds of motor outputs, different kinds of feedback networks, and so on, than finding a mate or finding food. Because of these unique requirements, I think different systems of the brain are going to be involved in the different kinds of emotions.

A related point is that emotion systems, like the fear system, didn't come about to create feelings (like the feeling of being afraid when in danger). I think feelings came much later in evolution. All animals have to be able to detect and respond to danger, regardless of the kind of cognitive architecture they have. This is as true of bees and worms and snails, as it is of fish, frogs, birds, rats, and people. Fear conditioning, by the way, occurs in all animals. And in all those that have an amygdala, the amygdala appears to be the key. The list at this point includes reptiles, birds, and a host of mammals, including humans. I think it's safe to say fear behavior preceded fear feelings in evolution. If so, feelings are probably the wrong thing to focus on when we study emotions. In this sense, animals were unconscious, unfeeling, and non-linguistic before they were conscious, feeling, and linguistic. It's too bad that we define the more basic processes as the negation processes that typify the human brain. It's possible that once consciousness and feelings came along that new kinds of emotions specifically tied to these evolved. But I'm trying to understand the things about emotions that are similar in humans and other animals so that I can work on emotions through the brain.

I tend to agree with theorists who say there are basic emotions that are hard-wired into the brain's architecture, and that one of the advantages of having an extra big cortex is that we can blend different hard-wired emotions together to create softer emotions, where cognitions come into play in a major way. For example, while detection and responding to danger may be built into the brain, the capacity to be afraid of falling in love is something that requires the cognitive integration of the system for finding mates and the system for defending against predators. While I'm sympathetic towards the basic emotions view, I don't really ascribe to it. It requires that you state what the different emotions are. That just leads to arguments. I'd rather spend my time worrying about one well accepted emotion and its organization in the brain than fighting over whether this or that mental process is an emotion or not.

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