The bacterium, the fly and the sugar bowl

[A response to Anthony Cashmore’s article denying free will published in the March 9, 2010 edition of the Proceedings of the National Academy of Sciences.]

I wasn’t sure if I was meant to take it seriously.  But it was being published in the Proceedings of the National Academy of Sciences (PNAS), it was even an Inaugural Article by a recently elected member… and it wasn’t yet April 1.  But there I was, reading in this august journal that

not only do we have no more free will than a fly or a bacterium, in actuality we have no more free will than a bowl of sugar.[1]

Does a fly have any more free will than…

As if that wasn’t shocking enough, this University of Pennsylvania biologist, Anthony Cashmore, was actually suggesting that our lack of free will should be reflected in our criminal justice system and proposing various adjustments to it.  Finally, to make matters even more disconcerting, a letter appeared a couple of weeks ago in PNAS, not taking issue with Cashmore on free will, but taking  our lack of it as a given, and discussing the implications for our system of justice.[2]

I guess I shouldn’t have been so shocked.  After all, this utter rejection of free will in the name of scientific reductionism has been around for at least a couple of centuries.  It’s as though Calvin’s doctrine of predestination was re-born but without God in the driver’s seat.  It was back in 1814 that Pierre-Simon de Laplace notoriously wrote in his Essai philosophique sur les probabilités:

A mind that in a given instance knew all the forces by which nature is animated and the position of all the bodies of which it is composed, if it were vast enough to include all these data within his analysis, could embrace in one single formula the movements of the largest bodies of the universe and of the smallest atoms; nothing would be uncertain for him; the future and the past would be equally before his eyes.[3]

… a bowl of sugar?

And for the past two centuries, wannabe Calvinists who found themselves in science rather than theology have kept up their attack on the notion of free will.  A hundred years after Laplace, it was celebrated biologist Jacques Loeb who found himself on the frontline of the assault, writing in his bestseller The Mechanistic Conception of Life:

Living organisms are chemical machines, possessing the peculiarity of preserving and reproducing themselves… We eat, drink and reproduce not because mankind has reached an agreement that this is desirable, but because, machine-like, we are compelled to do so.[4]

Perhaps Cashmore sees himself as the new century’s storm trooper for predestination; he certainly provided enough historical quotations himself to show that he is well aware of the pedigree of his idea.  And to give him credit, he has added an important stochastic element to the traditional notion of determinism, proposing that “there is a trinity of forces —genes, environment, and stochasticism (GES)—that governs all of biology including behavior, with the stochastic component referring to the inherent uncertainty of the physical properties of matter.”

But I intend to show that, in fact, Cashmore is so far from the truth that his statement above about the bacterium, fly and the bowl of sugar should be turned around completely to read:

not only we, but also a fly or a bacterium, in actuality have more free will than a bowl of sugar.

Cashmore cites, as evidence of his argument that GES governs all our activity, a number of recent studies showing that our conscious awareness of what we’re doing generally follows, rather than precedes, the relevant neural activity in the brain.  I agree with him that these studies are important, so let’s take a look at one of those he cited, by Soon et al., called appropriately enough “Unconscious determinants of free decisions in the human brain.”[5]

As Cashmore notes, Soon et al. conclude that

Taken together, two specific regions in the frontal and parietal cortex of the human brain had considerable information that predicted the outcome of a motor decision the subject had not yet consciously made. This suggests that when the subject’s decision reached awareness it had been influenced by unconscious brain activity for up to 10 s… Also, in contrast with most previous studies, the preparatory time period reveals that this prior activity is not an unspecific preparation of a response. Instead, it specifically encodes how a subject is going to decide.

So what does that conclusion tell us?  That certain parts of our brain – including part of our prefrontal cortex which is generally regarded as the locus of our “executive function” – make a decision and begin implementing it before our self-awareness becomes conscious  of this decision.  Is that evidence against free will?  No.  Rather, it’s evidence that when you, as an organism, decide to do something, that decision process is far more complex than we have generally understood it to be, and the part of the process that you’re conscious of is only a small, and sometimes relatively insignificant, part.  What Cashmore has done in his interpretation is conflate “conscious” with “free,” and therefore conclude that because we’re not conscious of something, we’re not free in our volition.

Cashmore is, of course, not alone in doing so.  In fact, even though he believes himself liberated from Cartesian dualism, he’s actually still confined within the modern dualistic tradition of Western thought that began with Descartes’ cogito ergo sum (“I think, therefore I am”) – the identity of self with one’s conscious awareness.  This tradition itself is really just a scientific rendering of an older current of thought that began with Plato two and a half millennia ago, when the eternal soul was conflated with the reasoning faculty and separated ontologically from the mortal body.

As cognitive linguists Lakoff & Johnson have shown, this split of self-identity between subject and object is so embedded in our thought and culture that it infuses the structure of our ordinary language. When we say “I pulled myself together,” or “I’m disappointed in myself,” or dozens of other such constructs, we’re exhibiting “something deep about our inner experience, mainly that we experience ourselves as split.”  Lakoff & Johnson generalize this as a dichotomy between the Subject, which they define as “the locus of consciousness, subjective experience, reason, will, and our ‘essence,’ everything that makes us who we uniquely are,” and multiples Selves, which “consist of everything else about us – our bodies, our social roles, our histories, and so on…”[6]

With the perspective of Lakoff & Johnson’s Self/Subject split,  we can interpret Soon et al.’s study as identifying some of the neural correlates of that split.  If one of the participants described the findings as “I wasn’t aware of the decision I’d made ten seconds earlier,” then rather than undermine the notion of free will, this merely demonstrates that the “specific regions of frontopolar and parietal cortex” that were seen to encode the decisions were not simultaneously participating in the conscious awareness of self.  In fact, a number of studies have searched for the neural correlates of that “self-referential or introspectively oriented mental activity,” and while acknowledging that it’s “likely to be widely distributed,” have identified the dorsal medial prefrontal cortex as probably the most important locus of the Subject/Self dynamic.

The important takeaway from all this is that, as Antonio Damasio has eloquently stated, “the mind exists in and for an integrated organism… The organism constituted by the brain-body partnership interacts with the environment as an ensemble, the interaction being of neither the body nor the brain alone.”[7] At this point, I can imagine Cashmore exultantly responding: “Right, so forget the distinction between conscious and unconscious processing, in the end it makes no difference.  Both the body and the brain are still subject to the determining factors of GES.  Neither is free.”  And from this perspective, I can agree with Cashmore that as far as free will goes, we humans are in the same bucket as his fly and bacterium.  Sure, there’s a extended continuum, and our higher-order consciousness may affect our actions more than Soon’s experiment shows, but  on a radical level, whether free will exists or not is really a question for the human, the fly and bacterium – all of us are in this together.

So let’s take a close look at the dynamics that all living organisms share.  Are we really subject to GES and nothing more?  This is where I think Cashmore’s understanding comes up short.  He states:

Some will argue that free will could be explained by emergent properties that may be associated with neural networks. This is almost certainly correct in reference to the phenomenon of consciousness. However… in the absence of any hint of a mechanism that affects the activities of atoms in a manner that is not a direct and unavoidable consequence of the forces of GES, this line of thinking is not informative in reference to the question of free will…

Well, the thing is, there’s no “absence of a hint of a mechanism.”  In fact, there’s a rigorous, interdisciplinary approach to the complexities of life, with decades of modeling under its belt, which recognizes the emergent properties of complex, self-organized systems as a dynamic which supersedes the forces of GES, while remaining consistent with the physics of these forces.  Cashmore betrays a possible lack of understanding of the nature of self-organized systems when he refers approvingly to “studies that indicate that consciousness is something that follows, and does not precede, unconscious neural activity in the brain.”  In fact, the breakthrough in understanding consciousness as an emergent property of neuronal self-organization is that there is no linear progression.  Consciousness neither follows nor precedes neural activity in the brain.  Consciousness is simultaneously both a function of and a driver of that neural activity.

How can that be?  The key concept necessary for an understanding of any living system – whether it’s human consciousness, a multi-cellular fly or a single-celled bacterium – is the two simultaneous directions of causation, both upwards and downwards.  This is summarized well by renowned neuroscientist György Buzsáki:

emergence through self-organization has two directions.  The upward direction is the local-to-global causation, through which novel dynamics emerge.  The downward direction is a global-to-local determination, whereby a global order parameter ‘enslaves’ the constituents and effectively governs local interactions.  There is no supervisor or agent that causes order; the system is self-organized.  The spooky thing here, of course, is that while the parts do cause the behavior of the whole, the behavior of the whole also constrains the behavior of its parts according to a majority rule; it is a case of circular causation.  Crucially, the cause is not one or the other but is embedded in the configuration of relations.[8]

This global order parameter, while influenced by genes and environment, and subject to stochastic variation, nevertheless exerts an emergent force on its own integrated system that is not determined by the parts of that system, but by the dynamic interactions of the whole with the parts.  Philosopher Evan Thompson, referring to empirical examples of epileptic patients changing the neurodynamic patterns of epileptic activity, explains that

‘downwards’ (global-to-local) causation is no metaphysical will-o’-the-wisp, but a typical feature of complex (nonlinear) dynamical systems, and may occur at multiple levels in the coupled dynamics of brain, body and environment, including that of conscious cognitive acts in relation to local neural activity.[9]

At this point, there’s a temptation to respond that, while the workings of these complex, self-organized systems are, for all practical purposes impossible to determine, they’re still deterministic.  However, this blanket dismissal of emergence fails to differentiate between what’s been termed “epistemological” and “ontological” emergence.  Philosophers Silberstein & McGeever explain the distinction well.  Epistemological emergence is the kind of “false” emergence that can be dismissed by determinists, where there’s no real top-down causation, but the system is just practically impossible to predict:

Most cases of emergence are epistemological. These are often cases in which it is hopeless to try to understand the behaviour of the whole system by tracing each individual part or process: we must find a method of representing what the system does on the whole or on average in a manner which abstracts away from causal detail… This kind of explanation often involves high-level descriptions of one sort or another: examples include averaging, gas laws and statistical mechanics in general.

A property of an object or system is epistemologically emergent if the property is reducible to or determined by the intrinsic properties of the ultimate constituents of the object or system, while at the same time it is very difficult for us to explain, predict or derive the property on the basis of the ultimate constituents. Epistemologically emergent properties are novel only at a level of description.[10]

Boiling water does not represent true, ontological emergence.

So, for example, if you heat a pot of water until it starts boiling, it’s sometimes claimed that the boiling is an emergent property of the water.  Wrong.  That’s epistemological emergence.  In practical terms, you’ll never be able to predict each bubble, but in principle, as Laplace said back in 1814, a mind that knew all the forces of nature could theoretically model the movements of the water.  Ontological emergence, by contrast, refers to

features of systems or wholes that possess causal capacities not reducible to any of the intrinsic causal capacities of the parts nor to any of the (reducible) relations between the parts. Emergent properties are properties of a system taken as a whole which exert a causal influence on the parts of the system consistent with, but distinct from, the causal capacities of the parts themselves.[11]

In other words, a “causal influence… consistent with, but distinct from” Cashmore’s GES.  Ontological emergence, in the view of Silberstein & McGeever, “entails the failure of part-whole reductionism.”  It also entails the failure of Cashmore’s denial of free will.

Perhaps the best explanation of ontological emergence I’ve come across is Evan Thompson’s description of the cell (and life) in terms of what he calls “dynamic co-emergence”:

An autonomous system, such as a cell or multicellular organism, is not merely self-maintaining, like a candle flame; it is also self-producing and thus procures its own self-maintaining processes… Whether the system is a cell, immune network, nervous system, insect colony, or animal society, what emerges is a unity with its own self-producing identity and domain of interactions or milieu, be it cellular (autopoiesis), somatic (immune networks), sensorimotor and neurocognitive (the nervous system), or social (animal societies).

Dynamic co-emergence best describes the sort of emergence we see in autonomy.  In an autonomous system, the whole not only arises from the (organizational closure of) the parts, but the parts also arise from the whole.  The whole is constituted by the relations of the parts, and the parts are constituted by the relations they bear to one another in the whole.  Hence, the parts do not exist in advance, prior to the whole, as independent entities that retain their identity in the whole.  Rather, part and whole co-emerge and mutually specify each other.

Biological life, seen from the perspective of autopoiesis, provides a paradigm case of dynamic co-emergence.  A minimal autopoietic whole emerges from the dynamic interdependence of a membrane boundary and an internal chemical reaction network.  The membrane and reaction network (as well as the molecules that compose them) do not pre-exist as independent entities.  Rather, they co-emerge through their integrative, metabolic relation to each other.  They produce and constitute the whole, while the whole produces them and subordinates them to it.[12]

Fruit flies exercising their free will.

Which is why I’m claiming free will not just for us humans, but also for that fly and bacterium.  In fact, speaking of flies, I’d refer Cashmore to a study by neurobiologist Bjorn Brembs who was attempting several years back to see if fruit flies in a deprivation chamber would fly in random or predictable patterns.  Turns out, they were neither random nor predictable.  They showed all the hallmarks of chaos, the form of activity that can arise from complex self-organized behavior, and which has been modeled in human brain patterns:  “It’s a rudimentary sort of free will,” Brembs concluded.[13]

Of course, I’m not claiming that we have the same amount of free will as a fly.  I think we’re at different points along a continuum of free will, which can be understood as a function of the complexity of the organism: whether it’s multicellular,  has a nervous system, a brain, a neocortex or (as in humans) a highly evolved prefrontal cortex.  In all cases, our free will is certainly constrained by Cashmore’s GES: genes, environment and stochasticism, but the constraints don’t eliminate free will, they just structure how it can be manifested.  One way of thinking about Cashmore’s GES is like a scaffolding: you can view the structure as a set of prison bars eliminating your freedom, or you can view it like a set of gymnasium bars, which you can grab onto and swing from.  It’s your, er, … well, it’s your choice.

Ultimately, I’m afraid that the mechanistic view of determinism propagated by Cashmore and others merely indicates the poverty of the reductionist worldview as a vehicle for understanding complex, self-organized systems such as cells, organisms and the human mind.  We’re all in this life together.  And whereas we humans may be the only ones capable of reflecting and writing about it, we share our free will with every other living organism on the earth.  That’s something that I, for one, am happy about.


[1] Cashmore, A. R. (2010). “The Lucretian swerve: The biological basis of human behavior and the criminal justice system.” PNAS, 107(10), 4499-4504.

[2] McEvoy, J. P. (2010). “A justice system that denies free will is not based on justice.” PNAS 107(20)E81.

[3] Cited by Postman, N. (1993). Technopoly: the Surrender of Culture to Technology, New York: Vintage Books.

[4] Cited by Capra, F. (1982/1988). The Turning Point: Science, Society, and the Rising Culture, New York: Bantam Books; and Rensberger, B. (1996). Life Itself: Exploring the Realm of the Living Cell, New York: Oxford University Press.

[5] Soon, C. S., Brass, M., Heinze, H.-J., and Haynes, J.-D. (2008). “Unconscious determinants of free decisions in the human brain.” Nature Neuroscience, 11(5), 543-5.

[6] Lakoff, G., and Johnson, M. (1999). Philosophy in the Flesh: The Embodied Mind and its Challenge to Western Thought, New York: Basic Books, 268-9.

[7] Damasio, A. (1994). Descartes’ Error: Emotion, Reason, and the Human Brain, New York: Penguin Books, xx-xxi, 88.

[8] Buzsáki, G. (2006). Rhythms of the Brain, New York: Oxford University Press.

[9] Thompson, E. (2001). “Empathy and Consciousness.” Journal of Consciousness Studies, 8(5-7), 1-32.

[10] Silberstein, M., and McGeever, J. (1999). “The Search for Ontological Emergence.” The Philosophical Quarterly, 49(195:April 1999), 182-200.

[11] Ibid.

[12] Thompson, E. (2007). Mind in Life: Biology, Phenomenology, and the Sciences of Mind, Cambridge, Mass.: Harvard University Press, 64-5.

[13] Homes, B. (2007).  “Fruit flies display rudimentary free will.” New Scientist, 16 May 2007.

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