The readiness potential and the soul: what happens when you resect their seat in the brain?

Abstract

Libet’s demonstration that activity in the supplementary motor area precedes conscious decision making is widely considered to have put the final nail in the coffin of dualism. Neurosurgeon Rickard Sjöberg argues that SMA resections show that Libet’s findings are in fact irrelevant to the neuroscientific discussion about free will.

Almost five decades ago, John Eccles used neurophysiological studies suggesting that voluntary movement is preceded by activity in the supplementary motor area (SMA) to argue that mind and brain are separate entities. Half a decade later, the finding made by Benjamin Libet that SMA activity precedes conscious decision making would put the final nail in the coffin of this dualistic theory. Today, results of neurosurgical resections of the SMA demonstrate the futility of this debate, challenging the role of the ‘Libet-study’ as an iconic symbol of the triumph of monism over dualism.

In line with contemporary approaches to the mind–brain problem, dualism has been completely out of fashion in the neurosciences for almost half a century. Its last chance at resurrection may have been the ambitious attempt that the Australian neurophysiologist and Nobel Laureate John C. Eccles made when he, together with the philosopher Karl Popper, published the book The self and its brain in 1977.¹ Eccles’ most central empirical argument for dualism appears to have been a set of neurophysiological experiments presenting what he described as ‘a convincing demonstration that voluntary movements can be freely initiated independently of any determining influences that are entirely within the neuronal machinery of the brain’.¹

What the studies referenced by Eccles demonstrated was that when subjects are instructed to perform a simple motor movement such as a flick of the wrist at a time of their own choosing, a certain form of activity in the supplementary motor area (SMA) known as the ‘readiness potential’ (Fig. 1) will have started approximately half a second earlier.² To Eccles, the SMA-activity seemed to emanate from nowhere, and the only reasonable explanation for it appeared to be that it mirrored the decision-making of the soul. Based on this evidence, he arrived at the theory that the SMA is the point of contact between body and soul. It would thus appear that he seemingly had finally found a solution to the mind–brain problem raised by the work of the French philosopher Rene Descartes more than 300 years earlier, a solution that furthermore appeared to be grounded in solid empirical neuroscience.

Figure 1.

The readiness potential.

Perhaps I am not the only neurosurgeon that prefers not to think of the organ I operate in as the seat of my patient’s soul as I make surgical decisions. For almost 20 years after Eccles presented his theory, neurosurgical resections involving the SMA were exceedingly rare. As I began my clinical career in neuro-oncological surgery at the University Hospital of Northern Sweden in Umeå, I noted that the habit of avoiding SMA surgery was still prevalent. Such surgery was still considered dangerous and the area as a mysterious one. I furthermore eventually found out that Eccles, roughly 30 years earlier, got to know one of the towering neurosurgical figures at the clinic while visiting one of his former PhD students (then a professor of neurophysiology at Umeå University). Whether there was a link between these two facts I do not know.

Even as Eccles was welcomed by neurophysiologists and neurosurgeons at Umeå, and SMA surgery was avoided at most centres throughout the world, his theory was widely criticized by leading members of the international neuroscience community when it was first published.³

For instance, the philosopher Mario Bunge argued that the idea of separating the brain from the soul was as meaningful as the idea of separating digestion from the digestive organs. However, the final decisive blow to Eccles’ theory of SMA as the point of contact between body and soul came when the San Francisco neurophysiologist Benjamin Libet and his colleagues used an ingenious modification of the kind of experiment Eccles drew so heavily upon.

In the new version of the experiment, Libet and his colleagues were able to pinpoint the time at which volunteers felt that they made the decision to perform the studied action (i.e. the flick of the wrist). As it turned out, the feeling of having made a decision occurred approximately a quarter of a second after the initiation of the readiness potential.⁴ In one blow, the readiness potential had become worthless as neuroscientific proof that the soul is a phenomenon that is void of substance and working independently of the brain. If the readiness potential (as suggested by Eccles) mirrors the decision to perform an action it would rather appear that this decision is made by the SMA (i.e. the brain) before the ‘conscious mind’ is even aware that a decision has been made. It would also appear that the mind is then lured into believing that it made the decision itself.

The claim that the ‘Libet-experiment’ raises questions about the notion of free will would become the enduring legacy of the debate concerning the nature of the readiness potential. Meanwhile, Eccles’ dualistic theory would fade into obscurity and oblivion. However, as I began systematically accepting patients for low-grade glioma surgery of the SMA, I also decided to test the validity of the most dramatic interpretations of the Libet experiment, i.e. that the SMA activity which the readiness potential mirrors is what creates the presumably illusory feeling of ‘deciding’ to perform non-stimulus driven motor actions.

My patients would, in response to the surgery, all develop different aspects of the so-called SMA syndrome. This condition was first described in 1977 (the same year as Eccles published his theory) by Laplane et al.⁵ in three patients as a result of SMA resections. In the typical case, there is, after a resection in this area (Fig. 2), an initial phase of akinetic mutism, that is a complete inability to move or talk, even in response to pain stimulation. In the second phase, there are deficits in the ability of the patient to voluntarily initiate movement of the contralateral half of the body as well as difficulties in initiating speech. For instance, I have seen some of my patients unable to raise a leg from the bed even an inch (voluntary movement), while at the same time being able to stand and walk when put in an upright position (automatic movement). Similarly, some may be unable to answer the question ‘How are you today?’ (voluntary speech) but nevertheless be fully able to read out loud headlines from a newspaper held in front of them (automatic speech). In the final stage of the syndrome, which will typically occur a couple of weeks after the surgery, there is a more or less complete remission of these signs.

Figure 2.

Supplementary motor area resection.

The SMA syndrome, which was unknown when the readiness potential was discovered, certainly demonstrates that this area of the brain is involved in the regulation of voluntary movement. However, when we systematically asked patients with the condition about their ability to want to, or decide to, try and perform the actions that were impaired by the syndrome, the results were clear. All of them reported a subjective experience of making 100% effort to perform the movements. If there is a part of the brain where the decision and/or feeling of deciding to perform a simple motor action is made, it is not the SMA. Rather, it appears that it is the ability to execute decisions—not make decisions—that is impaired after SMA surgery. In findings that could be seen as consistent with this, we also observed that the SMA syndromes of our patients were parallelled by dramatic but reversible deficits in the regulation of executive function, as demonstrated by established neuropsychological tests.^6,7

It seems to me that our experiences of SMA surgery at Umeå, as well as similar experiences in a countless number of other centres (SMA resection has, over the past two decades, finally become routine at many neurosurgical clinics around the world), clearly demonstrate that the findings made by Libet et al. are in fact completely irrelevant to the neuroscientific discussion about free will.⁸ Interestingly, similar conclusions were reached by Schurger et al.⁹ in 2012, when they demonstrated that the curve of the readiness potential has the same properties as a leaky stochastic accumulator. Even though activity in the SMA typically precedes voluntary action and even though stimulation of the area may produce activity that can be misinterpreted as voluntary, the sense of conscious strategic decision making is not located in the SMA.

There might at times be a need amongst those who are observing neurosurgery for the first time to distance themselves from the enormity of what is happening in front of them by resorting to a dualistic notion of mind and brain as separate entities. This approach might also serve the neurosurgeon who wants to remain calm while facing a challenging procedure. But on a wider societal level, the fascination evoked by the idea that the soul may be a physical entity may be even more powerful than the emotional needs of neurosurgeons. The enormity of the fact that brain research is dealing with the substrate of the soul is not just inspiring; it even has the potential to invoke awe.

In line with this, the so called ‘Libet experiment’ has evolved from being some scientific data that might contribute to the understanding of the SMA to an iconic symbol of this awe. As pointed out by the neuroscientist Robert Sapolsky,¹⁰ the act of referring to the experiment during the past four decades has been transformed to a ritual of almost religious significance. The Libet experiment is no longer a collection of data. It is a mythical story about how empirical neuroscience once defeated a long forgotten dualistic theory. No neurosurgical procedures or neurophysiological findings will change that fact within the foreseeable future.

Biography

Rickard Sjöberg is a senior consultant in neurosurgery and an associate professor of neurosurgery and medical psychology. His main research interest lies in understanding and preserving brain function in the context of low-grade glioma surgery.

Competing interests

The authors report no competing interests.