An Objective Measure of Consciousness…?

By Neuroskeptic | December 22, 2011 10:20 am

Could a puff of air in the eye offer a way to evaluate whether someone is conscious or not?

Yes it could, say Cambridge’s Tristan Bekinschtein and colleagues in a new paper about Sea slugs, subliminal pictures, and vegetative state patients.

It’s all about classical conditioning of the kind made famous by Pavlov. This is learning caused by the pairing of two stimuli, one of them somehow meaningful (usually unpleasant). So if I were to ring a little bell before, say, pepper spraying you, and I did that repeatedly, you would probably close your eyes whenever I rang that bell. Or just punch me, but you see the point.

Anyway, the key is that there are two kinds of classical conditioning. In the unhelpfully named “delay” conditioning, the warning stimulus overlaps with the painful one. Like if I started ringing my bell, then kept ringing it while I sprayed you with my other hand. In other words, there is no delay between the two stimuli… I said it was badly named.

By contrast in “trace”, conditioning there is a delay – the warning stops shortly before the second stimulus. Bekinschtein et al argue that trace conditioning requires conciousness. While delay conditioning can occur without awareness of the link between the two stimuli, only conscious awareness can bridge the time gap in trace conditioning.

In trace experiments (in which rather than pepper spray, the unpleasant stimulus is just a puff of air in the eye), people who, when asked, can’t explain the relationship (“sound means puff”) don’t learn to blink when they hear the sound. But with delay conditioning, this “unconscious” conditioning can occur. Likewise, under anaesthesia, trace conditioning is lost.

At first glance this looks like a piece of psychological trivia, but it could have literally life-or-death consequences. If trace conditioning is a measure of concious awareness then it could be used as a way of working out whether brain-injured people in a “coma” or “vegetative state” are aware or not.

This paper is in fact a follow-up to the author’s own 2009 study showing that some people in a vegetative state do show trace conditioning – and the ones who did were more likely to subsequently wake up.

One snag is that the humble sea slug, Aplysia, can undergo trace conditioning, yet it is presumably not conscious, at least not in any recognizable sense.

But Bekinschtein et al say that trace conditioning is a product of convergent evolution. Alplysia can do it and we can do it, but we use different means to the same end. Their argument is that while in Alpysia trace conditioning is known to be dependent on just a handful of individual neurons in the creature’s tiny “brain”, in humans it requires an intact hippocampus (containing millions of cells). People with hippocampal damage, who suffer amnesia, also can’t do trace conditioning.

That’s a good point but does that mean such hippocampal patients aren’t conscious? That would be weird because, apart from the amnesia, they seem perfectly normal. Presumably they’re just not conscious of the relationship between things separated in time

Also, primitive pathways for conditioning might still exist in humans, able to reactivate under special conditions. They do acknowledge this with a discussion of experiments showing that trace conditioning in the absence of conscious awareness of the relationship can occur but only when the warning stimuli are “scary”, like pictures of snakes. They say that with generic, neutral stimuli there is no good evidence of unconscious trace conditioning, but this seems like a fairly fine distinction.

Ultimately, it’s a very nice idea but only more studies on “unconscious” patients will tell us whether it’s really able to measure consciousness in a useful way.

ResearchBlogging.orgBekinschtein TA, Peeters M, Shalom D, and Sigman M (2011). Sea slugs, subliminal pictures, and vegetative state patients: boundaries of consciousness in classical conditioning. Frontiers in psychology, 2 PMID: 22164148

CATEGORIZED UNDER: animals, methods, papers, philosophy
  • Bj√∂rn Brembs
  • Simon

    There is no requirement that one of the stimuli in classical conditioning should be unpleasant. In Pavlov's famous experiments, the ringing of a bell (usually termrd the CS, conditioned stimulus) was coupled with food (UCS, unconditioned stimulus – stimuli that inherently cause the organism to respond), causing the dogs to salivate.

    I'm guessing that the idea of UCS:es being unpleasant stems from its role in one of the most well known applications of classical conditioning, the learning theory of phobias and other anxiety disorders..?

    Thank you for the post, fascinating research!

  • petrossa

    One would be better off considering if it's in the patients interest to be kept 'alive' for an extended period of time.

    Whilst long term comatose revivals do happen, no one wakes up ready to walk the marathon to put it mildly.

    For that i thank my dutch government for giving ME the right to decide over life and death.

    But i guess it'll be a while before the rest 'civilization' becomes enlightened enough to reach that level.

    In France i have seen an ambulance crew reviving the heart of a 20 minute dead floater on the beach only to have him die a day later.

    People of 80+ years old with advanced livercancer being operated thrice for a bowel obstruction so they could die in agony slowly.

    Makes one very nauseous.

  • Zen Faulkes

    “One snag is that the humble sea slug, Aplysia, can undergo trace conditioning, yet it is presumably not conscious, at least not in any recognizable sense.”

    Animal consciousness is a tricky topic, and I wouldn't be writing off consciousness in invertebrates so quickly. The last few decades of research on animal cognition have certainly suggested invertebrates have much more complicated cognitive behaviours than previously expected.

  • pseudonymoniae

    Well damn. Too bad no one thought to ask H.M. whether or not he was conscious while he was still alive!

    Oh well, that's hindsight for you.

  • Neuroskeptic

    Simon: Quite right, fixed, thanks!

  • Neuroskeptic

    Zen: Maybe… and as a vegetarian I am all in favour of animals being conscious. Otherwise I would have been missing out on meat for no reason. But while I can see a cat or even a lizard having some kind of recognizable consciousness, I can't see what Aplysia, with just a few thousand cells, would be conscious of. It seems to me that if we're ascribing consciousness to Aplysia we ought to ascribe it to plants as well. They can “learn” and “decide” to grow in certain directions…just very slowly.

  • neuromusic

    “It seems to me that if we apply consciousness to X, we ought to apply it to Y (which is OBVIOUSLY not conscious)”

    While I'm not convinced that trace conditioning is a binary metric of whether a human/dog/aplysia/robot has consciousness, I appreciate the authors' attempt to define a clear behavioral metric that could be used without these kinds of “common sense” arguments and “hunches”.

    All trace conditioning requires is a bit of memory and a system to derive causality from the sequencing of events and use that information to predict future events based on a current state. And, to a certain extent, that ability does seem to capture much of what I think of when I think of consciousness.

    The key different here among animals with respect to conditioning is then the specificity of the training (what types of stimuli can be used for CS/US pairing?) and prediction (does the CS/US pairing generalize?) and the time course over which CS/US pairs can be integrated (which is a function of the memory of the system). This is a much broader space to explore than the “does the animal exhibit trace condition or not” approach, but maybe the boundaries of consciousness are similarly blurry. Perhaps the main question is “over what timescales can the CS be integrated for trace conditioning?” with those organisms exhibiting longer timescale sensitivity being therefore “more conscious”?

  • practiCal fMRI

    Fascinating. I like neuromusic's follow-up, too. I'm going to go off piste here and pick up the analogy the authors use in their intro: that of (animal) flight.

    Bees, birds and men wearing special suits all generate lift; an area of reduced pressure above the body that tends to counteract some of the gravity working in the opposite direction. Whether it's a glide like a squirrel or powered like a dragonfly, the ultimate result – lift – has the same physical mechanism in the medium (air). All that changes is the nature and magnitude of the pressure difference. (An aside: to argue that the dragonfly has to beat his wings to fly whereas an eagle can soar is to confuse the essential issue of the pressure difference. A helicopter uses rotary wings, a plane fixed wings. Both generate lift with different complexities but using *exactly* the same laws of physics.)

    Seen this way, even lift looks bally complex as a phenomenon, yet we can explain it quite easily with angles of attack, etc. When we get distracted with the shape of the wing or feathers over membranes, etc. then we lose the big picture and the ability to (easily) explain flight. Don't agree? Simply take the atmosphere out of the equation and neither bees nor squirrels nor men in winged suits can generate lift. (Unlike reaction engines, e.g. a rocket, in all these cases a medium “to push against” is essential.)

    So if I jump out of a plane wearing jeans and a tee shirt I surely fall to the ground. If, while doing so, I adopt the configuration of a “lifting body” such that I have an angle of attack to the relative wind and thus traverse a horizontal path relative to the otherwise vertical descent, then I have (as a matter of physical fact) generated lift. I am still falling, but am I not also, technically, flying?

    If I can make lift appear complex when it's really not, no wonder consciousness looks intractable! Or, to complete the analogy, why can't the consciousness of a sea slug be akin to the “flight” of a bloke trying to glide during free fall from a plane wearing just jeans and a tee shirt?

  • ramesam

    Neuroskeptic said: “Zen: Maybe… and as a vegetarian I am all in favour of animals being conscious.”

    Well, a simple question: whether it is a roach on the wall running away from the lizard or a stag in the forest running away from a pouncing tiger, they are “conscious” of the threat to their life. Does Alpysia not show any response to a threat to its life? I do not think it will offer itself to be killed. All living things respond in their own way.

    Perhaps there lies a clue to know whether a creature is “conscious” or not.

    The vegetative state patient being “conscious” is perhaps to be understood in a different way.

  • omg

    I wouldn't use 'conscious'. That's like saying a flapping butterfly caused a tsunami. Yeah maybe ? But can you be less sensational, be more specific? Surely there's a plethora of literature since Pavlov they could've focused on.. like temporal awareness, alert state pathways. Something less medical layman? You CPR into regaining consciousness, move fingers, blink eyes, this article doesn't make sense to me. Why sea slugs? If consciousness via trace conditioning is so generic like a sea slug.. never even knew sea slugs had a brain or be conditioned to do anything, should work on any species right? Garden slug, mice etc.

  • Eric Charles

    Agree with Zen and Ramisam, if we really started talking about consciousness coherently, we would likely find sea slugs and all sorts of other “lower” animals qualify conscious. The interesting question should be:

    “What are they conscious of? And should consciousness of those things make a difference in how we treat them?”

    I'm not sure what exactly sea slugs are conscious of, but they sure seem conscious of someone hitting their gills, while they don't seem to notice if a close relative dies in front of them. Meanwhile, most farm animals seem conscious of quite a wide variety of things. Problem is, the farm animals are really yummy (though it is worth noting that the well-treated ones are yummier)

  • trisbek

    Hi, Thanks for paying attention to what we think and say.

    Just a few points

    Since we wanted to determine awareness without the need of motor or verbal report in presumably unconscious patients (among other things) we looked for a method. Trace conditioning seemed perfect since it could test awareness (of the relation between the tone and the airpuff to the eye) by seeing whether there is anticipatory muscle predicted by the tone and before the puff (learning!).

    And yes we show some people with disorders of consciousness learn and some others do not. And we and others have replicated these results in now more that 80 patients.

    But the theoretical problem stands and this Opinion paper in Frontiers was an attempt to answer the classical comments we get from biologists (I am one) and psychologists (I am almost one of those).

    Aplysia is a classic neuroscience model and a very good one and a simple google search will show why.

    The standard criteria for a patient to be considered conscious is quite blunt ( and we took it as it is and tried to find a better method, more robust, independent of subjective eye and more sensitive.

    And sea slugs can learn trace but cannot speak to tell us that they know about the contingencies between stimuli. People can, and every time we found that some talking person (patient or normal participant) has learned trace conditioning we also see that they know about the relation between the CS+ and the puff. Not only us but tons of people including very nice work by Squire et al.
    The logic goes like this: if a patient shows learning it is either conscious of the contingency but cannot express it or it has the necessary brain networks to learn and will be conscious later. This is the heart of the one network or two networks for trace conditioning.

    And yes it is specific to the conscious report of the relation between stimuli, not for general consciousness. But if someone can learn that a tone is associated with a puff but the other tone it is not, this person can discriminate, and if they can tell you so then they are conscious. Maybe from very specific things, but conscious.

    Of course HM was conscious, he talked to you (enough conscious criteria for disorders of consciousness).
    But he did not show trace conditioning. And he could not report the relation between stimuli. And therefore he was not conscious of this thing. He could never be, he could not form declarative memories, and it seems to be that trace is considered a declarative memory. Exactly my point. Conscious? Yes, but from the present only. Patients who show trace but cannot speak can form memories. Declarative ones most probably. Are they conscious of what is going on instant by instant? I do not know.

    The scary stimuli to predict the puff it is not minor point. It has been shown that we react much quicker to threat that to neutral stimuli in many conditions, not only in trace learning. Not a fine line. We know that scary things activate superfast ancient pathways in the brain that bypass the sluggish PFC to generate immediate reactions (to protect us). A faint neutral tone does not active this pathways; if it is slowly, through association, learnt then it involves hippocampus and frontal cortex (many refs) and apparently, also requires awareness.

    Finally, it is not more study on patients what will give us the answer to whether trace can measure consciousness because it becomes a circular argument. If a vegetative state patient (presumably unconscious) shows learning that means either that is in fact conscious (this assumes trace needs awareness), or that unconscious patients can learn (trace does not require awareness). No, the answers will come from somewhere else. Stay tuned for more experiments on this, we are working on it.

  • Ivana Fulli MD


    You wrote:

    “(…)Finally, it is not more study on patients what will give us the answer to whether trace can measure consciousness(…)”

    Your test is cheap and keeping alive comatose people for life is incredibly expensive, in money and in suffering for the family agonizing about hopes of “waking up” for their loved one-not unfrequently a young person having had a horseriding or bicycle riding or crossing the street accident with a motor car.

    What about a big multicentric study involving every clients the neurosurgeons all over europe and the Americas are sending off the neurosurgery ward to long term residential care for “plantes vertes ( ornement green pot plants)” in French medical vernacular?

    and the doctors working in those long term residential care places will have the priviledge to be involved in good medical research:

    they will tell the world if your prediction is true and if those with a yes to the test are awaking more often than the other ones.

    Of course, those doctors will take the same good (or bad) care of every patients for they will be kept blind about the result of the test (you have to tell them that only sophisticated neurosurgeons could do it and pretend it is a sophisticated assesment needing a certain distance from the eyes and the hairdryer etc…)

    Luckily, Neuroskeptic wrote and rightly so:
    “At first glance this looks like a piece of psychological trivia, but it could have literally life-or-death consequences.”

    At times when ressources are scarce, the health politiciens relying on scientific advices you have to be sure that you use more subjects than the fRMI reseachers on female orgasm usinf a fzew female masturbating under an unpleasant noisy machinery prohibiting sex toys.

    Obviously, you are interested in findings reguarding more spiritualy elevated matters since you wrote also:

    “(…)it becomes a circular argument. If a vegetative state patient (presumably unconscious) shows learning that means either that is in fact conscious (this assumes trace needs awareness), or that unconscious patients can learn (trace does not require awareness).(…)”

    PS: petrossa, I respect your living will of sort and i trust you being an aspie to be true to your word if you were to become slowly demented but in Italy-for example- a lot of people think that even a comatose life is sacred and suicide a sin…Plus, more importanty to my mind I have witness personnaly doing pro bono work for elderly people that some changes their mind. My father in law was a GP,had done family planning in Tunisia after retirment and di many abortion all along his carreer and had always proclaimed that he will commit suicide since life with infirmity was not tolerable. He lost most of his sight and years later very slowly his brain power. He chan ged completely his mind and it was obvious when he couldn't see much that he could have kill himself since he had a cabinet full of drugs nobody emptied since he was clearly telling that he had changed his mind.



No brain. No gain.

About Neuroskeptic

Neuroskeptic is a British neuroscientist who takes a skeptical look at his own field, and beyond. His blog offers a look at the latest developments in neuroscience, psychiatry and psychology through a critical lens.


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