LSD: Mechanism of Action and Side Effects
Pharmacologist David Nichols on the psychedelics, hallucinogen persisting perceptual disorder, and therapeutic...
Voluntary action is a topic which has often seemed right at the very edge of science, almost inaccessible to scientific inquiry. I’d like to talk about some ways that we might begin to study scientifically this really important aspect of who we are and of our individual autonomy.
First, we need to begin with a definition of voluntary action or, I would say, a definition of volition. We can use the word ‘volition’ to mean the mental state and brain state which allows us to make voluntary actions, but it’s actually quite difficult to come up with a good definition of voluntary actions. In our everyday lives, we feel we know what we mean because we think that we can do what we want, we can decide on what we do, and our actions are up to us. If I feel like going to eat pizza, I will just go and eat pizza, and that’s fine; it was my decision. But when we try to look at the problem scientifically about what exactly this means, it becomes quite a lot harder.
There are different traditions of defining volition. The tradition in neuroscience is quite rigorous in some ways but unsatisfactory in others. In neuroscience, traditionally, people have distinguished between actions, which are reactions or responses to an external stimulus, and actions, which are internally generated, such as voluntary action. My decision that I’m just going to go and eat a pizza, that that’s up to me, is internally generated; it’s something that I decided to do, whereas a reaction would be an action which is triggered by some immediate, obvious, direct external stimulus. The classic example of a reaction is a reflex: if the doctor taps on my knee with a tendon hammer and evokes a movement of my leg, then that’s a reflex response because it seems as though there is nothing more in the action than there was in the stimulus.
But quite a lot of our actions don’t seem like that: they seem to go beyond the immediate stimulus information. It seems as though something inside me is adding the information about what to do, where to go, what the decision should be and translating that into action. That is interesting because it puts volition and voluntary action almost at the opposite end of the Pavlov tradition, which tends to see all of our actions as being responses to environmental stimuli, but it’s unsatisfactory because it doesn’t say what volition is; it just says what it is not.
So, voluntary action is not a response to a stimulus. But then what is the cause of it? Where does it come from? What is the cause of the voluntary action? In philosophy, they have an answer to that question, so they say that voluntary action is an action which we make for a reason. So the test in philosophy for volition is, can you ask a why question? Why did you do that? Why did you eat pizza? Why did you cross the road? And that’s quite tricky for us to study in the laboratory; it’s quite tricky for us to generate the reasons for autonomous action in a laboratory setting. In a laboratory, we can give people motivation to act; for example, we can say, would you rather press this button and earn one pound or press this button and earn two pounds? But somehow, that doesn’t seem to be very voluntary because everybody is going to choose the button that gets them two pounds. It seems as though it’s the stimulus; it’s the association with the value which is driving the action.
So it’s very, very tricky to think of situations which allow us to test this ‘up to me’ quality in the laboratory and that has been the tricky point about the history of studying volition scientifically. The field really developed largely by finding new ways to measure the processes in the brain that occur when we do make decisions that are up to us. It has not had so much success in trying to engineer or control the different ways that we can manipulate the situation and get people to make voluntary decisions. In 1965, Kornhuber and Deecke, in Freiburg, Germany, were able to record a potential, an electrical activity, by placing electrodes on the scalp.
They found that before a voluntary action there was a reliable gradual increase in brain activity which they called ‘the readiness potential’ (or ‘Bereitschaftspotential’ because they were working in German). This activity seemed to come from the frontal areas of the brain, just in front of the motor cortex which we actually use to move and it seemed to build up a gradual electrical potential around a second or so before the person made a voluntary action.
The instruction that they gave to their participants was to press a button whenever they feel like it, not when I tell you, but when they want to. That is quite a strange instruction which people sometimes find quite hard to understand, but let’s imagine that they just occasionally make an action without any stimulus telling them to do so. The readiness potential seems to be something like the buildup of preparation in the brain as the person gets ready, ready, go – and press the button.
So we now believe that we have a biomarker which can show us the emergence of voluntary action, but we have not had very good ways of understanding why this biomarker begins; why does the person decide to press the button now rather than one or two or three seconds later? We recently published a paper in which we tried to address this question of what are the reasons for a voluntary action using a slightly surprising task. In our task, we told people that they should watch the screen and they should wait until the dots that they could see on the screen started to move either to the left or to the right. If they move to the left, press the left button; if they move to the right, press the right button. But you might have to wait a very, very long time before the dots start to move. You might just stare at the screen for up to two minutes, waiting for the dots to move: that’s really boring, and if you get bored waiting, you can skip to the next trial by pressing both the left and the right buttons simultaneously.
The critical thing is that the action of pressing the left and the right button simultaneously is not a response to the stimulus: there are no dots moving on the screen telling you to press the left or the right button; it’s up to you to decide, ‘Now I’m going to press the button because I’m bored of waiting for the dots, I’m going to get to the next trial’. So that is the reason that is an action that is not stimulus driven: it’s an action which is voluntary in the classic neurophysiological sense because it’s not a reaction to any stimulus in the external world, but it’s an action that I make because I want to because I’m bored. It’s a little bit paradoxical that in this experiment, we end up reducing free will to boredom, but it does fit with the classical definition that some of our actions are stimulus-triggered, and some of them are internally generated. If you look at what happens before these skip actions that people make to get onto the next trial, you see the classic readiness potential; you see this gradual increase in electrical activity in the frontal motor regions of the brain, which builds up prior to the action.
But the really interesting thing that we found is that this pattern of build-up is not just a reliable average that you see when you look at many trials grouped together. You can also look at the variability, consistency, and reliability of brain activity, and as the voluntary action gets closer and closer and closer in time, the pattern of brain activity stabilizes, converges and begins to become more and more consistent. So, the readiness potential is not just a signal that you can see on average, but it also seems to be a pattern that the brain is trying to achieve before you make a voluntary action.
That seems to be relevant to an interesting question about whether our voluntary actions are purely random or whether they actually reflect some internal characteristic distinctive process in our brain. We make actions all the time and maybe these famous voluntary actions which we consider so important for our free will and for our individual autonomy are not controlled at all, maybe they’re just spontaneous bits of neural noise which we occasionally produce.
Now, if our voluntary actions were just noise, you would expect the brain to be doing all kinds of things before the action happens. There’d be no pattern, but our data showed that before this voluntary action, there was a reliable convergence on a stable brain pattern. You don’t just see a readiness potential in the average; you see the brain trying to produce a stable readiness potential pattern. That suggests to me that there is a distinctive precursor or process that precedes our voluntary actions. Our voluntary actions are not random: we can see this emergence of neural activity in the frontal areas of the brain when there is an internal reason to act (in our case, this rather funny reason: ‘I’m bored, so I’m going to make the action so I can do something else, get on to the next trial’).
But it means that we can talk about volition in a scientific way, and we can talk about voluntary actions and the underlying mental process of volition as part of our cognitive ontology. It means we’re talking about something, there’s a thing, a process that the brain is actually trying to implement, like perception, like memory, like emotion. I’m perhaps less sceptical about volition than many neuroscientists: many neuroscientists say, wow, we don’t have free will, and volition is not something that exists at all, and we can’t study it scientifically, so let’s not talk about it. That is the behaviourist tradition, the tradition going back to Skinner. But I think many of our actions are relatively independent of the stimulus environment in which we find ourselves. It’s difficult for you to predict exactly what I’m going to do or say next even though you have full access to the environment in which we’re speaking: now you can see exactly what environment I’m in. This unpredictability of human action is not just randomness, but it’s about the fact that each of us has reasons for acting. Most of these reasons may be quite simple; they may be things as simple as satisfying basic needs (hunger, thirst and boredom), but these are processes in the human brain. We can study their brain basis, and we can identify the activities that occur in people’s brains before they decide for themselves what to do.
So the future directions, I think, for this line of research are to continue to try to understand the biomarkers, the precursor processes in the brain that occur before we act, to try to understand whether different reasons for action, different motivations for action correspond to different classes of brain activity. The example that I gave was boredom, but we will often act for other reasons: we might act just because we are nice people, for example, and we want to help others. What is the brain basis of that? I would like to know because we should work on it.
But also, I think it will be important to understand when, during this precursor process that prepares our voluntary action and triggers our movement, we actually become conscious of what we’re about to do. When do we have an awareness of the actions that we’re going to take? That’s important because, classically, in our culture, actions are associated with consciousness: we think that we have the capacity to understand what we’re doing and to control it before we do it because we’re conscious of the actions that we’re about to make. All systems of law are based on the idea that you’re responsible for your actions because you know what you’re doing, and if it was stupid, you should have stopped yourself before you did it. But we don’t really understand how that works in the brain or, indeed, if it works in the brain. Some people think that brain science shows that the legal concept of responsibility is wrong. I think that’s hasty; I think that’s not true. But I would like to know what it is about the action that I’m about to take now, which makes me aware that I’m about to make it and which is possibly relevant to whether I should have made it or not.
So, our legal systems all depend on a notion of conscious free will, and I would like to know what is the thing that is processed in our brains which allows that to work (or not). I don’t think I really believe in a conscious free. Well, I don’t think we’re anywhere near as free as we think we are, but I think we might be conscious of our actions. I don’t think that our experience of our actions is just an illusion, and I’d like to know about how that conscious experience is related to the brain mechanisms of control because that’s very relevant to how our entire society works.
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