麻豆传媒

PARTS of Ann Arbor bring The Truman Show to mind, with their wood-frame houses and white picket fences. Home to the University of Michigan, the city oozes middle-class prosperity and security. So, while doing research there a decade ago, Sarah Garfinkel was shocked to discover that young veterans of wars in Iraq and Afghanistan felt terrified even in Ann Arbor. 鈥淚t broke my heart,鈥� she says. And it changed the course of her career.

Garfinkel was in Michigan to study the brain circuitry involved in persistent fear. But working with traumatised veterans, she realised two things. First, a safe environment didn鈥檛 help them feel less fearful. And second, their fear was physical as well as mental: their hearts were constantly racing, their pupils dilated, their palms sweaty. 鈥淚t seemed to me that what their bodies were doing was meaningful, but I was just scanning their brains,鈥� she says. So she set out to understand the body-mind connection.

Garfinkel, now at the University of Sussex, UK, discovered that our bodies have more influence over our minds than you might imagine. 鈥淥ur thoughts, feelings and behaviours are shaped in part by the internal signals that arise from our body,鈥� she says. But it goes beyond that. It is leading her and others to a surprising conclusion: that the body helps to generate our sense of self and is a key part of consciousness. This idea has practical implications in assessing people who show little sign of consciousness. It may also force us to reconsider where we draw the line between life and death, and provide a new insight into how consciousness evolved.

It has long been known that our internal organs have lives of their own. They generate electrical activity, which is conveyed by neurons to the brain. As a result, signals from your heartbeat, your breathing, the slow, regular pulses of your stomach and the state of your muscles are all represented in the brain鈥檚 electrical activity. The brain, in turn, regulates these functions. In other words, there is a neuronal loop in which nerve cells carry information from the organs up to the brain, and commands down to the organs.

However, in the 20th century, neuroscientists tended to ignore the body. They associated mental life exclusively with the brain 鈥� an approach epitomised by the 鈥渂rain in a vat鈥� thought experiment, in which a disembodied brain continues to have normal conscious experiences.

Things began to change at the turn of this century, when neuroscientist Antonio Damasio at the University of Southern California pioneered the field of embodied consciousness. 鈥淚 have been defending the idea that the body is a critical player in anything that has to do with mind,鈥� he says. For years, he was in a minority, but now a handful of researchers, including Garfinkel, have joined him in his quest for the bodily origins of our sense of self.

Their starting point is interoception, a sort of sixth sense that we have about what is going on in our own body. A simple way to measure interoception is to get someone to count their heartbeats over a fixed time and compare their count with the actual one measured by an electrocardiogram (ECG). People鈥檚 ability to do this varies a lot. Those who can sense their heartbeat most accurately tend to and are better at perceiving the emotions of others.

What is going on? To tease it out, the researchers needed a read-out of interoception in the brain. They found one in the brain鈥檚 response to the heartbeat, known as the heartbeat-evoked potential (HEP). Many studies focus on this because the HEP is relatively easy to measure: the heartbeat isn鈥檛 completely regular, so it is possible to filter the HEP out from all the brain鈥檚 other activity. The HEP can be found by simultaneously recording a person鈥檚 heartbeat, via an ECG, and scanning their brain. It shows up as activity in various 鈥渞esting-state networks鈥� in the brain, which are active even when a person isn鈥檛 consciously doing anything.

One clue as to what the HEP might be doing came in 2016 when neuroscientist Hyeongdong Park at the Swiss Federal Institute of Technology in Lausanne (EPFL) and his colleagues who were experiencing a full-body illusion. Volunteers donned a virtual reality headset and watched a simulation of themselves having their back stroked as it was being stroked in reality. After a while, they described feeling as if they were now physically located closer to where their virtual self was, rather than where they were actually sitting. The more pronounced their HEP, the stronger the illusion. Here was the first neurophysiological evidence of a link between interoception and the brain鈥檚 notion of self, claimed the researchers. 鈥淭he HEP reflects changes in bodily self-consciousness such as changes in self-identification with 鈥� and displacement towards 鈥� the virtual body,鈥� says Olaf Blanke, who heads EPFL鈥檚 Laboratory of Cognitive Neuroscience.

鈥淚t starts with interoception, a sort of sixth sense that we have about our own body鈥�

The EPFL group has gone on to show that our bodily self is anything but passive 鈥� it intervenes in every decision we make. Blanke鈥檚 team has built on work by US physiologist Benjamin Libet, who in 1983 detected a signal that arose in the brain just before a person became aware of their intention to act. Libet interpreted it as meaning that there is no such thing as free will. that the same signal is linked with a particular bodily act, breathing: we are more likely to initiate a voluntary act when exhaling. Blanke describes the finding as a clear indication that 鈥渁cts of free will are hostage to a host of inner body states鈥�.

Such experiments have led that signals from the organs, together with signals from the outside world, feed a representation of the bodily self to the brain. This includes self-identification and self-location, as in the full-body illusion. They also believe that the rhythmic nature of signals from the organs helps generate a feeling of your self being continuous in time. 鈥淭he cyclic pattern of the heartbeat is predictable,鈥� says Blanke, 鈥渁nd this temporal element could play a big role in that continuity of self.鈥�

Catherine Tallon-Baudry, a neuroscientist at the Ecole Normale Sup茅rieure in Paris, France, has a different conception of how the body contributes to self-consciousness. The brain is constantly bombarded by signals from inside and outside the body and as a result of its own cognitive processes. The signals are processed by different brain circuits. She thinks that rhythmic signals from the organs impose a unified frame of reference on the brain. This allows us to perceive all that incoming information from the perspective of a single, subjective 鈥淚鈥�. 鈥淚 think of consciousness as a property that is generated by the brain once it has integrated information from the whole organism,鈥� she says. And a series of experiments supports her contention, she believes.

In 2014, Tallon-Baudry and Park, who worked in her lab before he moved to Blanke鈥檚, began by of things. They asked people to fix their gaze on a central point and to say whether they could see a faint ring around that point. The bigger a person鈥檚 HEP just before showing them the ring, the more likely they were to perceive it. 鈥淭he heartbeat behaves like an extra piece of visual information,鈥� says Tallon-Baudry. It also provides the intrinsic 鈥渕ineness鈥� of the conscious experience. 鈥淚n the person鈥檚 response 鈥� 鈥業 saw something鈥� 鈥� there is that element of 鈥業鈥�,鈥� she says. 鈥淲e shouldn鈥檛 ignore that element of 鈥業鈥� in perception.鈥�

Blanke sees this study as a beautiful demonstration of the threshold of consciousness, but says there is no need to conclude that the self is involved. To address this issue, Tallon-Baudry and her group This time, they homed in on the distinction between 鈥淚鈥� and 鈥渕e鈥�. Tallon-Baudry says 鈥淚鈥� captures the most basic aspect of self 鈥� the aspect that comes before thought, the unified entity that does the thinking. It is fundamentally different from the kind of reflection about 鈥渕e鈥� that implies monitoring different bodily functions without that sense of unity.

To see if they could show that the brain treats those two concepts differently too, Tallon-Baudry鈥檚 team asked people who were having their brain scanned to fixate on a point and then let their mind wander. Every now and then, they were interrupted and asked whether 鈥� at that precise moment 鈥� they were thinking about 鈥渕e鈥� or 鈥淚鈥�, which they had been trained to recognise. Depending on which they reported, the HEP occurred in different parts of the brain: a region near the front for 鈥渕e鈥� thoughts and one further back for 鈥淚鈥� thoughts. This showed for the first time that the brain does indeed discern between the two concepts.

In as-yet unpublished work, Tallon-Baudry鈥檚 group has also shown how the body might contribute to our decisions on our personal preferences, which in many ways define us in the eyes of others. Volunteers saw 200 posters of well-known films and were asked to rate the ones they had seen. Next day, they were shown pairs of posters from the films they had rated, and had to indicate which they preferred as they had their HEP tracked. As is usual with these sorts of experiments, people鈥檚 responses weren鈥檛 wholly consistent. However, people with the biggest HEP at the moment of choice gave answers that were most in line with their original ratings. Their choices were truest to themselves when their brains were listening most closely to their hearts.

Blanke鈥檚 notion of a bodily self and Tallon-Baudry鈥檚 notion of bodily consciousness may not be too far apart. Indeed, they can imagine hitting on an overarching model of the embodied self that reconciles their findings. But how does Garfinkel鈥檚 research fit in?

Emotional me

She has been exploring two connected ideas: that bodily signals influence emotions and that emotions shape our sense of self through memory and learning. Working with people with autism, she has concluded that the problems they often encounter relating to others stem from their brains being overwhelmed with the visceral inputs associated with their own and others鈥� emotion. Building on the idea of an overactive body-brain axis, Garfinkel鈥檚 research has now come right back to what haunted those traumatised war veterans: fear. In , she has adapted a classic psychology paradigm called fear conditioning, in which volunteers learn to associate neutral stimuli with negative consequences. She measured people鈥檚 heartbeats and their skin鈥檚 electrical conductivity, which increases when we feel fearful. Her volunteers showed more fear when stimuli were presented as their heart was contracting than when it was relaxing. The phase of the heartbeat also affected how easily those fear responses were evoked later on. 鈥淭hese signals from the heart can really drive and override conditioned fear responses,鈥� she says.

Garfinkel doesn鈥檛 like to talk about consciousness because she thinks the concept is woolly. 鈥淐onsciousness operates on so many levels,鈥� she says. But she does believe she is trying to solve the same puzzles as Blanke and Tallon-Baudry. For Damasio, all three approaches are reconcilable if we take an evolutionary perspective.

鈥淚t may force us to reconsider where we draw the line between life and death鈥�

Four billion years ago, the first primitive organisms monitored changes in their bodily state 鈥� equivalent to hunger, thirst, pain and so on 鈥� and had feedback mechanisms to maintain equilibrium. The relic of those primitive mechanisms is our autonomic nervous system, which controls bodily functions such as heartbeat and digestion, and of which we are largely unconscious. Then, about half a billion years ago, the central nervous system, featuring a brain, evolved. 鈥淚t was an afterthought of nature,鈥� says Damasio. But it became the 鈥渁nchor鈥� of what had once been a more distributed mind. Changes in bodily state were projected onto the brain and experienced as emotions or drives 鈥� the emotion of fear, say, or the drive to eat. Subjectivity evolved later again, he argues. It was imposed by the musculoskeletal system, which evolved as a physical framework for the central nervous system and, in so doing, also provided a stable frame of reference: the unified 鈥淚鈥� of conscious experience.

While Damasio contemplates a synthesis, the other researchers are thinking about applications of their findings. Garfinkel intends to test her idea about an overactive heart-brain axis directly in people affected by trauma. Already, her results lend support to the rationale that drugs designed to act on the cardiovascular system might help treat post-traumatic stress disorder 鈥� and indeed such drugs are .

Blanke and Park have filed a patent related to the use of breathing patterns to predict behaviour. Among other applications, it could help in tuning brain-computer interfaces to be more sensitive to the choices of people with disabilities.

Tallon-Baudry is working with neurologist Steven Laureys at the University of Li猫ge in Belgium to study the HEP in people with disorders of consciousness, such as coma. They have trained an artificial intelligence to learn how the HEP relates to measurable clinical signs in such patients, to test whether the HEP alone could serve as a diagnostic tool in people whose clinical signs are ambiguous 鈥� particularly those in the grey area known as minimally conscious state.

There are philosophical implications to these discoveries too. If consciousness is embodied, that could affect how we think about death, which is currently defined by the World Health Organization as the irreversible loss of brain (but not body) function. The research also has implications for the consciousness of other animals and how we treat them. And if consciousness is embodied, it would mean that a machine or robot with no way of integrating signals from its body will never be truly conscious. 鈥淲hen you start to think through the implications of the embodied self,鈥� says Tallon-Baudry, 鈥渢hey are really quite profound.鈥�