New Scientist Magazine. 22.03.10
STEVEN LAUREYS will always remember the 21-year-old woman who had had a stroke. She had been taken to a hospital in Liège, Belgium, where her condition worsened rapidly. She soon lost all motor movement, even the ability to open her eyes. Her prognosis looked bleak, so her doctors turned to Laureys, a neurologist, for a final opinion before turning off her ventilator.
By recording her brain activity as she was asked to respond to simple tasks, such as counting the number of times her name was spoken in a random string of first names, Laureys confirmed that the woman was aware of her surroundings, and so she remained on life support (Neurocase, vol 15, p 271). Clearly that was the right decision: a year later she had recovered enough to be discharged from hospital. "It was only technology that permitted us to show that she was conscious," says Laureys of the University of Liège.
There had, however, been another clue to the patient's active mental state - too tentative to hold any weight in the diagnosis, but nevertheless significant. Laureys had observed a signature of coordinated neural activity, present in the resting patient, which seems to appear in the brain of anyone who is conscious. While such readings may one day provide a better diagnosis of coma patients, their ultimate implications may be even more profound, providing evidence for a 30-year-old theory that claims to explain consciousness itself.
Consciousness is one of neuroscience's long-standing mysteries. At its most basic, it is the simple question of why we become aware of some thoughts or feelings, while others lurk unnoticed below conscious perception. Is there a single module in the brain, a "seat of consciousness" if you like, that is responsible for awareness? Or is it a result of more complicated activity across a number of brain regions? Solve this, and we may be a little closer to explaining the more esoteric aspects of our complex internal experience.
Now one theory that claims to do just that is rapidly gaining weight, with strong evidence from research such as Laureys's to back up its predictions. The idea, dubbed the global workspace theory, was first floated in 1983 by Bernard Baars of The Neuroscience Institute in San Diego, California. He proposed that non-conscious experiences are processed locally within separate regions of the brain, like the visual cortex. According to this theory, we only become conscious of this information if these signals are broadcast to an assembly of neurons distributed across many different regions of the brain - the "global workspace" (see diagram) - which then reverberates in a flash of coordinated activity. The result is a mental interpretation of the world that has integrated all the senses into a single picture, while filtering out conflicting pieces of information (see "Neural conflicts").
The 'global workspace' integrates the senses into a single picture, filtering out conflicting information
Lack of compelling evidence left the idea languishing on the shelf. Indeed, it took more than 15 years for the theory to prove its mettle, when Stanislas Dehaene of the French National Institute of Health and Medical Research (INSERM) in Gif sur Yvette and Jean-Pierre Changeux of the Pasteur Institute in Paris updated Baars's model with the latest findings on the brain's wiring. Dehaene's group had already shown that distant areas of the brain are connected to each other and, importantly, that these connections are especially dense in the prefrontal, cingulate and parietal regions of the cortex, which are involved in processes like planning and reasoning.
Considering Baars's theory, the team suggested that these long-distance connections may be the architecture that links the many separate regions together during conscious experience. "So, you may have multiple local processes, but a single global conscious state," says Dehaene. If so, the areas with especially dense connections would be prime candidates for key regions in the global workspace.
The team put the theory to the test in 2005 by studying a neurological phenomenon known as "inattention blindness", where we fail to see things that are before our eyes. They presented their volunteers with two strings of letters in quick succession. In some instances, they had to answer a question about the first stimulus just after they had seen it, which caused them to miss the second string of letters and only perceive them non-consciously.
By placing 128 electrodes on their volunteers' scalps, Dehaene's team teased out the differences in neural activity when they were conscious of the second stimuli, and when it escaped their attention. For the first 270 milliseconds the neural activity was roughly the same in both cases. After that there were stark differences. The neurons quickly stopped firing if the letters were perceived unconsciously. But when the subjects were conscious of the letters, the neurons in a number of brain regions thought to be part of the global workspace, including the frontal and parietal lobes, exploded into synchronous activity (Nature Neuroscience, vol 8, p 1391). "Suddenly, your brain ignites with additional activation, particularly in the frontal lobes, when you are conscious," says Dehaene.
This explosion of coordinated activity was just what Baars had proposed, corresponding to the widespread "broadcast" of signals across the global workspace that he predicted would accompany conscious perception.
Encouraged by this preliminary evidence, Dehaene's team decided to put the global workspace model through its paces again. This time, volunteers were shown a number (the target), which appeared at one of four locations on a computer screen. After a random delay, the computer blanked out the original number and placed four letters around the original location. If the delay was less than 50 ms, the change becomes too confusing for the brain to process, and it cannot consciously detect the target. Any longer than 50 ms, though, and the subjects were aware of the target.
A signature of consciousness
The team measured the subjects' neural activity with scalp electrodes as they completed the task. As expected, conscious perception coincided with a burst of activity in some of the regions implicated in the global workspace model, spanning the frontal, parietal and temporal brain regions. What's more, the researchers again found a 300 ms delay between presenting the stimuli and witnessing this explosion of neural activity (PLOS Biology, vol 5, p e260).
This 300 ms delay is one of the theory's key predictions, since you would expect any signals to take a while, relatively speaking, to reach the different parts of the global workspace, before we are fully aware of perceiving something.
Further evidence arrived last year, when Dehaene's team studied people with damage to their prefrontal cortex, which should disrupt the long-distance connectivity in the global workspace. They would therefore take significantly longer to become conscious of the information, as it would have to find its way through alternative, longer routes. And that's exactly what they found, with the patients taking around 18 ms longer to become aware of the stimuli (Brain, vol 132, p 2531). The same was true for people with multiple sclerosis, who also have extensive damage to their nerve connections, particularly in the prefrontal cortex (NeuroImage, vol 44, p 590).
Compelling as these results are, the real proof of the pudding for any theory in neuroscience comes from precise measurements of brain activity taken by electrodes implanted in the brain - the most accurate technique available. Such evidence arrived in 2009, when Raphael Gaillard, who was working in Dehaene's lab and is now at the University of Cambridge, and his colleagues took the opportunity to test the conscious perception of patients with epilepsy, who had electrodes implanted in various regions of their brains as part of exploratory surgery.
As in the previous experiments, brain activity during both conscious and unconscious perception was similar for the first 300 ms, followed by increased and coordinated activity in distant parts of the brain whenever something was perceived consciously. Crucially, although the electrodes had been placed in areas relevant to the treatment of epilepsy - and not specifically areas proposed to be important in conscious perception - 68 per cent of the electrodes still recorded a significant response to the conscious stimulus. This suggests that the global workspace may in fact occupy a significant chunk of the cortex.
It was the most compelling evidence yet for the "signature of consciousness" predicted by the global workspace theory. Baars was elated. "I'm thrilled by these results," he said at the time. "It is the first really solid, direct evidence for the notion of conscious global access, or global broadcasting." More detailed experiments have supported these results by looking at the activity of single neurons (see "Consciousness, one neuron at a time").
Following these advances, researchers like Dehaene and Laureys are now attempting to ask more nuanced questions thrown up by the global workspace theory. An important question from a clinical perspective, for example, is how the signatures of consciousness might differ between people with brain damage and the healthy population.
Laureys thinks he has some answers. Certain regions of the brain's global workspace, dubbed the default mode network (DMN), are active even when we are resting and not concentrating on any particular task. If the global workspace really is essential for conscious perception, Laureys's team predicted that the activity of the DMN should be greatest in healthy volunteers and in people with locked-in-syndrome, who are conscious but can only move their eyes, and much less active in minimally conscious patients. Those in a vegetative state or in a coma should have even less activity in the DMN.
The researchers found just that when they scanned the brains of 14 people with brain damage and 14 healthy volunteers using fMRI. In a paper published in December 2009, they showed that the activity of the DMN dropped exponentially starting with healthy volunteers right down to those in a vegetative state (Brain, vol 133, p 161). "The difference between minimally conscious and vegetative state is not easy to make on the bedside and four times out of 10 we may get it wrong," he says. "So this could be of diagnostic value."
Even more important, Laureys thinks that a person's DMN could one day determine their prognosis. "I'm predicting those with a higher level of DMN activity will be the ones who will recover from their coma, or vegetative states, or minimally conscious states," he says.
Those with a higher level of activity in certain brain areas will be the ones who recover from their coma
He cautions that neuroscientists have to be "humble and honest" in their search for the neural basis of consciousness, since many questions remain. We still don't know the exact chain of activity within the global workspace, for example, or what information the brain regions are communicating to each other. "These neurons are electrical units in a chemical soup, and we have not yet decoded their language," says Laureys.
Then there are the philosophical questions to consider. Philosophers like David Chalmers at the Australian National University in Canberra, tend to divide the study of consciousness into the so-called hard and easy problems. The easy problem looks at correlations between brain activity and different states of consciousness - something the global workspace theory is beginning to crack. The hard problem, meanwhile, probes the deeper question of how these patterns of electrical activity could ever give rise to the many subjective facets of our internal life that we experience as conscious human beings.
Indeed, philosophers like Chalmers remain unconvinced that we are even close to approaching a solution to the hard problem. Dehaene, however, predicts that it will all fall into place once we have a comprehensive global workspace theory to work with. "Once the easy problem is solved, there will be no hard problem," he says.
Consciousness, one neuron at a time
Rodrigo Quiroga at the University of Leicester, UK, may be famous for identifying the individual neurons that fire in response to the actress Jennifer Aniston, but his technique of using very small and precise electrodes to record the activity of single neurons has unearthed even greater treasures: patterns of single neuron activity that result in either non-conscious or conscious perception.
Quiroga's team worked with people with epilepsy who were undergoing surgery to treat their condition. The researchers were interested in neurons in the medial temporal lobe (MTL), which is known to be involved in the transformation of perceptions into memories. Since you would expect conscious perceptions to be stored in long-term memory, the group suspected the MTL may be part of the global workspace network underlying consciousness.
As with other such tests, the patients were shown a target image followed by a mask, another image that is meant to confuse the brain's perception of what it has just seen. Importantly, the delay between the target image and the mask controls whether the subject becomes conscious of the target or not. When the volunteers reported perceiving the image, Quiroga's team found that certain MTL neurons fired about 300 milliseconds after the target stimulus. The same neurons never fired at that late stage when the stimulus was processed non-consciously (Proceedings of the National Academy of Sciences, vol 105, p 3599). This all-or-nothing response of single neurons is predicted by the global workspace model, providing some of the strongest evidence for the theory.
Although it's not yet known whether all the neurons in the relevent brain areas are roped into the global workspace, or just a subset, the ease with which Quiroga found them does at least suggest they are very prevalent.
Neural conflicts
The global workspace model of consciousness, proposed by Bernard Baars of The Neuroscience Institute in San Diego, California, argues that non-conscious perceptions are processed in relatively small, local areas of the brain. It is only when this information is broadcast to a network of neural regions, the "global workspace", that we become conscious of whatever it is that we are experiencing. That, of course, relies on the ability of the brain to prevent conflicting messages from separate regions of the brain from being broadcast to the global workspace, which would confuse our picture of the world. "The reason why one needs a single coherent interpretation is because you need to broadcast it, and you don't want to broadcast competing messages at the same time," says Baars.
This could have been a deal breaker for Baars's theory, but luckily so-called binocular rivalry experiments provide good evidence that the brain does indeed actively select which information to send to our consciousness. Normally, both our eyes see the same scene, so the brain can easily combine the two monocular inputs into a coherent picture. But present the left eye with an image that's dramatically different from what the right eye is seeing, and experiments have revealed the brain resolves this conflict by allowing you to only see one or the other image at any one time. In other words, you are only conscious of either the left-eye image or the right-eye image, but never both simultaneously.
Anil Ananthaswamy is a consulting editor for New Scientist.
By recording her brain activity as she was asked to respond to simple tasks, such as counting the number of times her name was spoken in a random string of first names, Laureys confirmed that the woman was aware of her surroundings, and so she remained on life support (Neurocase, vol 15, p 271). Clearly that was the right decision: a year later she had recovered enough to be discharged from hospital. "It was only technology that permitted us to show that she was conscious," says Laureys of the University of Liège.
There had, however, been another clue to the patient's active mental state - too tentative to hold any weight in the diagnosis, but nevertheless significant. Laureys had observed a signature of coordinated neural activity, present in the resting patient, which seems to appear in the brain of anyone who is conscious. While such readings may one day provide a better diagnosis of coma patients, their ultimate implications may be even more profound, providing evidence for a 30-year-old theory that claims to explain consciousness itself.
Consciousness is one of neuroscience's long-standing mysteries. At its most basic, it is the simple question of why we become aware of some thoughts or feelings, while others lurk unnoticed below conscious perception. Is there a single module in the brain, a "seat of consciousness" if you like, that is responsible for awareness? Or is it a result of more complicated activity across a number of brain regions? Solve this, and we may be a little closer to explaining the more esoteric aspects of our complex internal experience.
Now one theory that claims to do just that is rapidly gaining weight, with strong evidence from research such as Laureys's to back up its predictions. The idea, dubbed the global workspace theory, was first floated in 1983 by Bernard Baars of The Neuroscience Institute in San Diego, California. He proposed that non-conscious experiences are processed locally within separate regions of the brain, like the visual cortex. According to this theory, we only become conscious of this information if these signals are broadcast to an assembly of neurons distributed across many different regions of the brain - the "global workspace" (see diagram) - which then reverberates in a flash of coordinated activity. The result is a mental interpretation of the world that has integrated all the senses into a single picture, while filtering out conflicting pieces of information (see "Neural conflicts").
The 'global workspace' integrates the senses into a single picture, filtering out conflicting information
Lack of compelling evidence left the idea languishing on the shelf. Indeed, it took more than 15 years for the theory to prove its mettle, when Stanislas Dehaene of the French National Institute of Health and Medical Research (INSERM) in Gif sur Yvette and Jean-Pierre Changeux of the Pasteur Institute in Paris updated Baars's model with the latest findings on the brain's wiring. Dehaene's group had already shown that distant areas of the brain are connected to each other and, importantly, that these connections are especially dense in the prefrontal, cingulate and parietal regions of the cortex, which are involved in processes like planning and reasoning.
Considering Baars's theory, the team suggested that these long-distance connections may be the architecture that links the many separate regions together during conscious experience. "So, you may have multiple local processes, but a single global conscious state," says Dehaene. If so, the areas with especially dense connections would be prime candidates for key regions in the global workspace.
The team put the theory to the test in 2005 by studying a neurological phenomenon known as "inattention blindness", where we fail to see things that are before our eyes. They presented their volunteers with two strings of letters in quick succession. In some instances, they had to answer a question about the first stimulus just after they had seen it, which caused them to miss the second string of letters and only perceive them non-consciously.
By placing 128 electrodes on their volunteers' scalps, Dehaene's team teased out the differences in neural activity when they were conscious of the second stimuli, and when it escaped their attention. For the first 270 milliseconds the neural activity was roughly the same in both cases. After that there were stark differences. The neurons quickly stopped firing if the letters were perceived unconsciously. But when the subjects were conscious of the letters, the neurons in a number of brain regions thought to be part of the global workspace, including the frontal and parietal lobes, exploded into synchronous activity (Nature Neuroscience, vol 8, p 1391). "Suddenly, your brain ignites with additional activation, particularly in the frontal lobes, when you are conscious," says Dehaene.
This explosion of coordinated activity was just what Baars had proposed, corresponding to the widespread "broadcast" of signals across the global workspace that he predicted would accompany conscious perception.
Encouraged by this preliminary evidence, Dehaene's team decided to put the global workspace model through its paces again. This time, volunteers were shown a number (the target), which appeared at one of four locations on a computer screen. After a random delay, the computer blanked out the original number and placed four letters around the original location. If the delay was less than 50 ms, the change becomes too confusing for the brain to process, and it cannot consciously detect the target. Any longer than 50 ms, though, and the subjects were aware of the target.
A signature of consciousness
The team measured the subjects' neural activity with scalp electrodes as they completed the task. As expected, conscious perception coincided with a burst of activity in some of the regions implicated in the global workspace model, spanning the frontal, parietal and temporal brain regions. What's more, the researchers again found a 300 ms delay between presenting the stimuli and witnessing this explosion of neural activity (PLOS Biology, vol 5, p e260).
This 300 ms delay is one of the theory's key predictions, since you would expect any signals to take a while, relatively speaking, to reach the different parts of the global workspace, before we are fully aware of perceiving something.
Further evidence arrived last year, when Dehaene's team studied people with damage to their prefrontal cortex, which should disrupt the long-distance connectivity in the global workspace. They would therefore take significantly longer to become conscious of the information, as it would have to find its way through alternative, longer routes. And that's exactly what they found, with the patients taking around 18 ms longer to become aware of the stimuli (Brain, vol 132, p 2531). The same was true for people with multiple sclerosis, who also have extensive damage to their nerve connections, particularly in the prefrontal cortex (NeuroImage, vol 44, p 590).
Compelling as these results are, the real proof of the pudding for any theory in neuroscience comes from precise measurements of brain activity taken by electrodes implanted in the brain - the most accurate technique available. Such evidence arrived in 2009, when Raphael Gaillard, who was working in Dehaene's lab and is now at the University of Cambridge, and his colleagues took the opportunity to test the conscious perception of patients with epilepsy, who had electrodes implanted in various regions of their brains as part of exploratory surgery.
As in the previous experiments, brain activity during both conscious and unconscious perception was similar for the first 300 ms, followed by increased and coordinated activity in distant parts of the brain whenever something was perceived consciously. Crucially, although the electrodes had been placed in areas relevant to the treatment of epilepsy - and not specifically areas proposed to be important in conscious perception - 68 per cent of the electrodes still recorded a significant response to the conscious stimulus. This suggests that the global workspace may in fact occupy a significant chunk of the cortex.
It was the most compelling evidence yet for the "signature of consciousness" predicted by the global workspace theory. Baars was elated. "I'm thrilled by these results," he said at the time. "It is the first really solid, direct evidence for the notion of conscious global access, or global broadcasting." More detailed experiments have supported these results by looking at the activity of single neurons (see "Consciousness, one neuron at a time").
Following these advances, researchers like Dehaene and Laureys are now attempting to ask more nuanced questions thrown up by the global workspace theory. An important question from a clinical perspective, for example, is how the signatures of consciousness might differ between people with brain damage and the healthy population.
Laureys thinks he has some answers. Certain regions of the brain's global workspace, dubbed the default mode network (DMN), are active even when we are resting and not concentrating on any particular task. If the global workspace really is essential for conscious perception, Laureys's team predicted that the activity of the DMN should be greatest in healthy volunteers and in people with locked-in-syndrome, who are conscious but can only move their eyes, and much less active in minimally conscious patients. Those in a vegetative state or in a coma should have even less activity in the DMN.
The researchers found just that when they scanned the brains of 14 people with brain damage and 14 healthy volunteers using fMRI. In a paper published in December 2009, they showed that the activity of the DMN dropped exponentially starting with healthy volunteers right down to those in a vegetative state (Brain, vol 133, p 161). "The difference between minimally conscious and vegetative state is not easy to make on the bedside and four times out of 10 we may get it wrong," he says. "So this could be of diagnostic value."
Even more important, Laureys thinks that a person's DMN could one day determine their prognosis. "I'm predicting those with a higher level of DMN activity will be the ones who will recover from their coma, or vegetative states, or minimally conscious states," he says.
Those with a higher level of activity in certain brain areas will be the ones who recover from their coma
He cautions that neuroscientists have to be "humble and honest" in their search for the neural basis of consciousness, since many questions remain. We still don't know the exact chain of activity within the global workspace, for example, or what information the brain regions are communicating to each other. "These neurons are electrical units in a chemical soup, and we have not yet decoded their language," says Laureys.
Then there are the philosophical questions to consider. Philosophers like David Chalmers at the Australian National University in Canberra, tend to divide the study of consciousness into the so-called hard and easy problems. The easy problem looks at correlations between brain activity and different states of consciousness - something the global workspace theory is beginning to crack. The hard problem, meanwhile, probes the deeper question of how these patterns of electrical activity could ever give rise to the many subjective facets of our internal life that we experience as conscious human beings.
Indeed, philosophers like Chalmers remain unconvinced that we are even close to approaching a solution to the hard problem. Dehaene, however, predicts that it will all fall into place once we have a comprehensive global workspace theory to work with. "Once the easy problem is solved, there will be no hard problem," he says.
Consciousness, one neuron at a time
Rodrigo Quiroga at the University of Leicester, UK, may be famous for identifying the individual neurons that fire in response to the actress Jennifer Aniston, but his technique of using very small and precise electrodes to record the activity of single neurons has unearthed even greater treasures: patterns of single neuron activity that result in either non-conscious or conscious perception.
Quiroga's team worked with people with epilepsy who were undergoing surgery to treat their condition. The researchers were interested in neurons in the medial temporal lobe (MTL), which is known to be involved in the transformation of perceptions into memories. Since you would expect conscious perceptions to be stored in long-term memory, the group suspected the MTL may be part of the global workspace network underlying consciousness.
As with other such tests, the patients were shown a target image followed by a mask, another image that is meant to confuse the brain's perception of what it has just seen. Importantly, the delay between the target image and the mask controls whether the subject becomes conscious of the target or not. When the volunteers reported perceiving the image, Quiroga's team found that certain MTL neurons fired about 300 milliseconds after the target stimulus. The same neurons never fired at that late stage when the stimulus was processed non-consciously (Proceedings of the National Academy of Sciences, vol 105, p 3599). This all-or-nothing response of single neurons is predicted by the global workspace model, providing some of the strongest evidence for the theory.
Although it's not yet known whether all the neurons in the relevent brain areas are roped into the global workspace, or just a subset, the ease with which Quiroga found them does at least suggest they are very prevalent.
Neural conflicts
The global workspace model of consciousness, proposed by Bernard Baars of The Neuroscience Institute in San Diego, California, argues that non-conscious perceptions are processed in relatively small, local areas of the brain. It is only when this information is broadcast to a network of neural regions, the "global workspace", that we become conscious of whatever it is that we are experiencing. That, of course, relies on the ability of the brain to prevent conflicting messages from separate regions of the brain from being broadcast to the global workspace, which would confuse our picture of the world. "The reason why one needs a single coherent interpretation is because you need to broadcast it, and you don't want to broadcast competing messages at the same time," says Baars.
This could have been a deal breaker for Baars's theory, but luckily so-called binocular rivalry experiments provide good evidence that the brain does indeed actively select which information to send to our consciousness. Normally, both our eyes see the same scene, so the brain can easily combine the two monocular inputs into a coherent picture. But present the left eye with an image that's dramatically different from what the right eye is seeing, and experiments have revealed the brain resolves this conflict by allowing you to only see one or the other image at any one time. In other words, you are only conscious of either the left-eye image or the right-eye image, but never both simultaneously.
Anil Ananthaswamy is a consulting editor for New Scientist.
