Why do lemons taste sour? The puzzle of innate qualia.

A really nice recent paper reported the identification of a family of proteins that seem to act as sour taste receptors. They are expressed in our taste buds and allow us to detect the positively charged hydrogen ions produced by acidic substances. This is important because it lets us identify foods that are unripe or spoiled by bacterial growth, like sour milk. The discovery of these sour receptors is a big step forward – it adds to our understanding of how different kinds of chemicals are detected in the sensory neurons of the tongue and processed in the brain. But it leaves one really big question unanswered – why do sour things taste like that?

 Image credit: http://www.funcage.com/blog/babies-tasting-lemons-for-the-first-time/

Why does eating a lemon produce that specific reaction – the scrunched up face, puckered lips, eyes squinting, head drawn back, eyebrows raised in surprise? This is an incredibly universal and apparently innate reaction – you can see it in unsuspecting babies eating lemons for the first time (to great comic effect). It’s not just humans, either – you can see something roughly similar in the way dogs react when they taste lemons (again, worth a look just for kicks and giggles). 

That very specific response to that very specific stimulus is clearly wired into our nervous systems. Now, maybe that’s not that amazing – we have lots of reflexive responses to various stimuli that are pre-wired into our neural circuitry, like withdrawing your hand from a hot stimulus, for example. You could imagine programming that kind of thing into a robot.

But I think we can say something much more profound – that the qualitative nature of the experience of eating lemons is somehow wired into our nervous systems. In fact, you might even say that the qualia associated with that experience are in effect encoded in our genomes, as this is where the instructions are to wire the nervous system in such a way that entails that response. 

I’m on shaky ground, here, I know, making inferences about subjective states. However, I think we can say, first off, that even babies and dogs are having an experience when they eat a lemon and react that way. Given that the outward signs of that experience are so universal, I see no good reason to think that the subjective experience is likely to differ between individuals – it certainly seems more parsimonious to expect that it wouldn't. The experience that babies and dogs have will not be exactly like the one adult humans would have, of course, but it seems likely that there must be some shared perceptual primitive that is the basis for this experience.

How could this possibly be established? How is the system wired to drive this kind of perceptual experience?

Wired for taste

The anatomical system for detecting and discriminating tastes is now quite well understood. Taste and smell are our two chemical senses and they have quite different jobs to do. Our sense of smell is all about detecting and discriminating between a huge range of different chemicals, each of which smells different to us. We have thousands of different odorant receptor proteins that do that job – each one specialised to bind to a different chemical. The taste or gustatory system is quite different – rather than discriminating, it instead lumps things together into just six or seven broad categories (that we know of): sweet, bitter, sour, salty, fatty, and savoury (and maybe carbonated).

Image credit:  http://blogs.discovermagazine.com/scienceandfood/tag/taste-receptor/#.Wqo154IuA4w

These categories refer in one sense to the chemical properties of the substances being tasted (the “tastants”) and, in another, to the nature of the perceptual experience they induce. Sugars, salts and fats are all types of molecules with specific chemical properties, which are detected by specialised proteins expressed in the taste buds. The taste of savouriness (or “umami”) is induced by the chemical monosodium glutamate, which is present in things like meats and cheeses. And things that taste sour are chemically acidic – they produce positively charged hydrogen ions, which is what sour receptors detect. (Since hydrogen atoms are made up of one proton and one electron, a positively charged hydrogen ion is simply a proton).

Compounds that taste bitter are an exception – they do not necessarily share a specific chemical property or structure. They are, in fact, extremely chemically diverse – the one thing they have in common is that they may be toxic to us and should be avoided if we don’t want to poison ourselves. Animals have therefore evolved a large family of bitter taste receptor proteins, capable of detecting a wide range of such chemicals, but the taste system does not discriminate between them – that’s the job of the olfactory system. The taste system simply codes them all as “bitter”, sounding a general alarm that they should be avoided.

The thing that links the chemical properties of these tastants to the perceptual experiences of sweetness, bitterness, etc., is the way the taste receptor neurons are wired into the brain. Each of our taste buds contains a dozen or more taste receptor neurons. Each one of these neurons expresses exclusively just one of the types of taste receptor proteins – sweet receptors, or bitter receptors, or sour receptors and so on.

Image credit:  http://blogs.discovermagazine.com/scienceandfood/tag/taste-receptor/#.Wqo154IuA4w

This exclusivity is the key, because it means each taste receptor neuron responds to only one class of tastants. So the brain just has to figure out which neurons were activated to know what kind of chemical was detected. That is accomplished by specifically wiring the different kinds of taste receptor neurons into different regions of the gustatory cortex in the brain, creating labelled lines for each taste.

A set of primary sensory neurons associated with the facial and glossopharyngeal cranial nerves innervate the taste receptor cells in the tongue and send another projection into the brainstem. Cells from that area of the brainstem project onwards to a specific part of the thalamus (a central subcortical structure which acts as a relay station for lots of types of sensory information). And cells from this ventral posterior nucleus of the thalamus project in turn to the primary gustatory cortex, which is located near the front of the brain.

The important thing in all this wiring is that the different types of taste receptor neurons get selectively wired into distinct subregions of the primary gustatory cortex. Despite being intermingled and distributed across the surface of the tongue, the nerves carrying information for each taste get segregated as they project into the brain, so that, ultimately, the different tastes are mapped across the gustatory cortex. 

This is what that looks like in mouse cortex:

And in humans: 

The mechanisms that direct this selective wiring are not fully understood but some of the molecules responsible for the very first wiring "decision" - which sensory neurons innervate which taste receptor neurons - have recently been discovered. They are members of the semaphorin gene family (my favourite!) that are used as connectivity labels in many areas of the developing nervous system. 

In this way, the coding of tastes gets transformed from a distributed set of different cell types in the periphery into a segregated spatial map in the brain. Now the rest of the brain just has to know which part of the gustatory cortex is active to know which type of chemical was detected. That’s a nice, even elegant, system for coding chemical tastants in the brain. An observer looking at patterns of brain activity could probably even infer what taste someone was detecting.

The problem is, there is no such observer inside the brain. The logic of the anatomy doesn’t really tell us anything about how specific patterns of neural activity in those areas give rise to conscious, subjective percepts. And it certainly doesn’t explain the qualitative nature of these percepts.
Where is the sourness of lemons perceived?

If we go back to our lemons, here’s what we know so far: the protons produced by citric acid are detected by these newly discovered specialised proteins, which are expressed by dedicated taste receptor neurons, which eventually send information, through converging connections, via several relays, to the “sour” domain of the gustatory cortex. That’s all important information, but we might ask: at what point along this pathway does perception actually occur?

Clearly, if we just stimulated the tongue, but it wasn’t connected to the brain, you would not perceive anything (in the same way that you wouldn’t see anything if your optic nerves were destroyed, even though your retina might still be electrically responding to light). And if the gustatory regions of the brainstem or of the thalamus were activated, but not connected to the cortex, my guess is you wouldn't perceive anything either.

Now, what about the primary gustatory cortex? If you stuck an electrode in there and gave it a zap, you might well induce a taste percept. Indeed, cross-activation of gustatory cortex might underlie certain forms of synaesthesia, where various stimuli in other sensory or conceptual modalities – like words or musical notes, for example – induce strong, involuntary taste percepts.

But, again, if primary gustatory cortex were activated and not telling any other part of the brain about it, you probably wouldn’t perceive anything. In fact, you can see the problem that arises with this kind of thinking – you keep on passing the signal from one station to the next, but you never reach any area that could possibly do the job of perception all by itself. The mistake is to think that perception just entails feedforward propagation and processing of sensory stimuli from the periphery. This leads to an infinite regress. There is no final station in the brain that “does conscious perception”. 

Instead, we should think of perception as a comparison between incoming sensory stimuli and an internal model of the world, which is instantiated in widespread activity patterns across the brain. This comparison of bottom-up signals with top-down expectations can lead to an updating of the model to accommodate new information, which, (in some way that remains completely mysterious) may constitute the act of perception. This kind of process necessarily involves information flowing in both directions and neuronal activity reverberating through multiple cortical areas and subcortical regions, such as the thalamus.

The point of all this is to enable the organism to infer what it is out in the world that is the source and explanation of the sensory stimuli it is receiving. In the case of taste, the inference is that there is something sour, or sweet, or bitter in your mouth and there are certain appropriate responses to those different stimuli.

So, all that (vague as it is) gets us a little further in understanding how perception may happen. It probably requires all kinds of additional weird recursiveness (in the vein of Douglas Hofstadter’s Strange Loops) to get conscious awareness out of the physical system of the brain. But let’s say, for argument’s sake, that those kinds of structures and system dynamics exist. Now, one of our specialised sour receptor proteins has bound a proton and, through the magic of all this distributed and recursive circuitry, we have perceived “sour” and can infer there is an acidic thing in our mouth.

But why are sour things sour?

But we still haven’t explained why sour things taste like that. This goes beyond the fact that mildly sour things are pleasant and attractive, while extremely sour things are unpleasant or aversive. It is not just a matter of attaching a positive or negative valence for the organism to the sensations or the casual stimuli. Again, that kind of thing can be implemented in a robot, without it involving any qualitative experience.

If we assume that tasting lemons really does involve a very particular, common, or even universal, qualitative experience, then there is something else (a very big something!) that we still have to explain. (And, actually, if we assume the opposite – that the quality of the experience may vary across individuals – that only gives us more to explain). Where does the quality of this experience come from?

The chemical senses are unlike vision or touch or hearing. For those other senses, the stimuli have some properties that can be actively explored and that can be compared across the senses. They have statistical and physical properties and sensorimotor contingencies that in some way can inform the nature of the attendant visual or tactile or auditory percepts. Information from each sense can also be used to calibrate responses in the others, especially as babies and infants grow and explore their world – calibrating their visual system based first on things they can touch and only later on things at a distance. You can even think of vision as a skill – one that we get better at with experience.

Some people hold that because that kind of “ecological information” is always available in the environment, we don’t even really have to have internal representations of these stimuli. I wouldn’t go that far myself, but it is certainly true that many aspects of the phenomenal experience of visual or tactile or auditory stimuli are experience-dependent, integrative, and responsive to active exploration (enactive and embodied).

This really isn’t the case for the chemical senses. The phenomenology of smell or taste doesn’t map in any sensible way to the properties of the stimulus (unlike for audition or vision). There is no physical property of a proton that in any way relates to the properties of the sour percept it induces. And it’s also not experience-dependent or learned or calibrated versus the other senses. When you smell or taste something – especially for the first time – there is no reference point, no perceptual anchor, no sensorimotor contingencies – it just is like that.

Somehow, the quality of that experience is entailed in the wiring of the gustatory system, and the way it is linked to other areas of the brain. Which means, ultimately, that it is entailed in the program in the genome that directs that wiring. In a brain that is wired that way, detecting protons with your taste buds just will lead to that kind of subjective experience that feels like that. Those qualia are somehow innate and nothing we know (maybe nothing we can know) about the anatomy and physiology of the system can even approach providing an explanation for that.

And that is doing my head in.


  1. Kevin,

    I'm a laymen re Philosophy of Mind, but I do work in the field of psychology. And I've read quite a bit of science and philosophy regarding the mind-body problem.

    This article you have written is one of the clearest, most-profound articles I've read on the topic. The ways in which you have clearly and concisely illustrated what we do and don't--and maybe, possibly, perhaps can't--know about the relationship between so-called objective, observable phenomena and so-called subjective, unobservable phenomena we know as subjective, conscious, experience.

    Thank you!

    P.S. I use the term 'so-called' because I do not believe these are ontologically distinct phenomena; just phenomena that can be experienced intrinsically and/or observed extrinsically.

  2. Random thought based on this piece from the article:

    >> "...it is certainly true that many aspects of the phenomenal experience of visual or tactile or auditory stimuli are experience-dependent, integrative, and responsive to active exploration (enactive and embodied).

    This really isn’t the case for the chemical senses."

    In light of this, it's interesting that smell and taste sensations seem to appear infrequently in dreams as compared to the other senses.


    >> "There is no physical property of a proton that in any way relates to the properties of the sour percept it induces. And it’s also not experience-dependent or learned or calibrated versus the other senses. When you smell or taste something – especially for the first time – there is no reference point, no perceptual anchor, no sensorimotor contingencies – it just is like that.

    Somehow, the quality of that experience is entailed in the wiring of the gustatory system, and the way it is linked to other areas of the brain."

    It may turn out that the full palette of phenomenal qualia can be mapped to neural networks, but it may turn out that a full map might require a model even more fine-grained than the neural level.

    This quote from physicist Laurence Krauss comes to mind:

    "The real world is quantum mechanical, at least as far as we can tell. All classical interpretations are just approximations of that quantum mechanical world, so they are all going to be “wrong”. The late physicist Sidney Coleman, who was the smartest guy when I was at Harvard, said we should really be talking about the interpretations of classical mechanics, because the world we live in is this approximation of reality. We should be talking about interpretations of that in terms of the underlying reality, instead of talking about interpretations of reality in terms of something that is just clearly wrong."

    Thus, while "the quality of [sour] experience is entailed in the wiring of the gustatory system," we must keep in mind that what we take to be the gustatory system is an approximation of reality.

    There's no doubt that elements of conscious experience can be modeled at the classical approximation level of neurons (for example, the trichromatic theory of color vision), but other qualities of experience may require models beyond classical physics.

    1. Very true - only a small percentage of people have tastes and smells in their dreams. That may well have to do with the fact that those qualia are far less linked to other aspects of experience.

      As for looking for an explanation of qualia at the quantum level, that feels like just appealing to something mysterious to explain something mysterious...

      On the other hand, we're clearly going to have to come up with something better than our current reductionist, feedforward models in neuroscience to explain qualia, consciousness in general and free will.

    2. It's not so much an appeal to QM as it is a recognition that the classical reality given to us in subjective, perceptual experience is in large part a product of our evolved, human perceptual systems. This is in no way a denial of a concrete, mind-independent reality, but only a recognition that our distinctly human, classic subjective experience of reality is a filtered, biased, approximation of external reality.

      While this perceptual system had allowed us to gain incredible insight into many structures and processes of reality, when the system is turned on itself, I'm dubious that it has the capacity to perceive its own underlying processes.

      When the perceptual system perceives itself, it doesn't see perceptions, it sees the brain.

    3. I agree that the self-regarding system is not necessarily aware of its own internal processes, but there may be a level at which the brain goes beyond just modeling what is out in the world and begins to model itself making that model. Whether that is the answer or not, we clearly *somehow* have to be having percepts, which have a qualitative nature to them. These are of course filtered, biased, selectively attended to, etc., but the point is we're having them. And they feel like something. And the example of sour taste is a striking one to illustrate the fact that the way they feel is somehow innate.

  3. The short outline of how taste works is nice (though explanations like that can be found all over, obviously). But the rest is problematic.

    So you say we can't follow the sequence of brain regions that process perceptual input to reach the region that does consciousness - that's a fair point to make, both empirically (no region found) and conceptually for a number of reason, like how sequences and areas of processing are a pretty lossy way of characterizing how the brain does stuff. How, though, does it follow now that consciousness involves the difference to a top-down model "which is instantiated in widespread activity patterns across the brain"? And how (or where) would that difference be registered?

    And how exactly does the visual percept map onto physical or statistical properties of the perceived in a way that a smell or a taste don't? You are talking about a relationship between a proton and the sourness perceived, but that does not appear like a very sensible unit of analysis, unless you want to map properties of photons to visual experiences. The more interesting relationship would be between from properties of a lemon to the lemon's taste and I don't see how that would categorically differ from the relationship to the lemon's visual appearance or the tactile sensations interacting with it causes.
    (Funny side note: You haven't really implied the opposite, but the sensorimotor contingencies are part of a theory of perception rather than percepts and the mental model you are mentioning is precisely what this theory is rejecting.)

    And in what sense are smell or taste not learned like vision? What did your first glass of red wine taste like? I'm assuming it didn't taste like a basket of red fruit, clove and dark chocolate, but instead it tasted like red wine. Why does vanilla make us perceive things as sweet even if they are not? Quite clearly, taste and smell (*exactly* like vision) are not some entailment of the genetic code, but a function of experience.

    1. How does the sensorimotor contingencies theory account for lucid dreaming or dreaming in general?

      Re learning: Are you suggesting that humans can learn to experience light wavelengths of 380–450 nm as, say, red (instead of the typical violet)? How about experiencing the protons in question as sweet or salty instead of sour? Are you suggesting this is learned and does not map onto the human sensory/nervous system?

      There's no doubt that humans posses the ability to flexibly cognitively frame perceptually experienced reality--and that it's not entirely fixed. And it's true that how we perceptually experience reality is also to an extent learned and malleable.

      However, to suggest that the majority of human phenomenal experience is contingent on the environment and learned is a mistake. We are humans after all and--despite our incredible adaptability--we will phenomenally experience and cognitively frame reality in ways that ultimately map onto our unique human nervous systems that evolved over billions of years.

    2. The world does not come parsed into separate things that we merely frame differently as we accumulate experience, the percepts we like to talk about are entities that do not actually exist in reality in any meaningful way. There are no sweet things in the world and there are no purple things either. Unless you want to go down to the quantum level, which obviously comes with its own own problems (let's not forget that our current understanding of physics is fundamentally inconsistent) and will unlikely further our understanding in any case, that's the position that we will have to start from: our perception is learned and contextual.

      Sure, there are physical or chemical processes that determine how the world is registered in terms of translating molecules in food or changes in air pressure into neural impulses, but that's just the (potential) input. Virtually all theories of what our brains do are based on information in one way or another. Yet information is not absolute, it is relative to what that information is supposed to be *about*, that is the things that we want to keep (or make) distinct. As different people make different experiences over the course of their lives and consequently need to distinguish different things, what they perceive ought to be different as well, as any "thing" that could be perceived will necessarily differ in how much information it provides.

      Visual and auditory "illusions" (they're not illusions once that point about learning is understood) should suffice to make this obvious for those senses and the vanilla example was meant to illustrate the same point for taste. For wine it is particularly apparent how our perception observably changes with experience, where more different wines that we experience and consequently learn to distinguish give rise to an increasing number of percepts like tasting cherry or smelling oak. And when you put people in a different context, say give them different price points for the bottle or change the colour of the wine, they will perceive different things.

      If our world was such that everything was the same colour or such that colour appeared randomly and changed all the time, then we should not perceive it, as it would have no information at all. That is an extreme case, clearly, and merely meant for illustration, but the same reasoning holds in a gradual fashion, such that we fade in or out of perceiving something contextually and over the course of our lives.

      So clearly, our conscious perception does not simply map onto the translation of physical inputs like protons into nerve impulses. It makes more sense to see that mechanism as a necessary condition for perception or a constraint on what *could* be perceived, as it would appear that the lack of a protein that binds to positively charged hydrogen atoms would not allow us to perceive bitterness. But, more importantly, if everything entering our mouths (including our saliva) had enough such atoms to saturate our receptors, we also could not perceive bitterness, as it wouldn't pick anything out (i.e. have no information) - just like we have no idea what our own spit usually tastes like, as it's always there and completely uninformative (unless we get sick maybe).

      Finally, adding sugar or acid to a dish can mellow out its bitterness and while you can point out that the mechanism behind is that the bitterness receptors respond in a different way, this does not actually matter for the argument, as it still means that this mechanism and hydrogen atoms do not form a useful unit of analysis for talking about consciousness and perception.

      There's a lot more to say about this, but this comment is already way too long and I will finish with a quote by William James from over a century ago, that is now as relevant as ever:

      (In a separate comment, there's a character limit.)

    3. The noticing of any part whatever of our object is an act of discrimination. Already on p. 404 I have described the manner in which we often spontaneously lapse into the undiscriminating state, even with regard to objects which we have already learned to distinguish. Such anæsthetics as chloroform, nitrous oxide, etc., sometimes bring about transient lapses even more total, in which numerical discrimination especially seems gone; for one sees light and hears sound, but whether one or many lights and sounds is quite impossible to tell. Where the parts of an object have already been discerned, and each made the object of a special discriminative act, we can with difficulty feel the object again in its pristine unity; and so prominent may our consciousness of its composition be, that we may hardly believe that it ever could have appeared undivided. But this is an erroneous view, the undeniable fact being that any number of impressions, from any number of sensory sources, falling simultaneously on a mind WHICH HAS NOT YET EXPERIENCED THEM SEPARATELY, will fuse into a single undivided object for that mind. The law is that all things fuse that can fuse, and nothing separates except what must. What makes impressions separate we have to study in this chapter. Although they separate easier if they come in through distinct nerves, yet distinct nerves are not an unconditional ground of their discrimination, as we shall presently see. The baby, assailed by eyes, ears, nose, skin, and entrails at once, feels it all as one great blooming, buzzing confusion; and to the very end of life, our location of all things in one space is due to the fact that the original extents or bignesses of all the sensations which came to our notice at once, coalesced together into one and the same space. There is no other reason than this why "the hand I touch and see coincides spatially with the hand I immediately feel."

      James, William (1890), The Principles of Psychology, Vol. 1, New York: Henry Holt.

    4. Thanks for your comments. To reply to the questions in your first one:

      1. The predictive inference model is just that - a model. It makes sense to me as a framework for how perception could work. In fact, it seems to me that it *must* work that way and there are decent models of how it could be instantiated anatomically (e.g., in feedforward and feedback circuits in neocortex that propagate predictions in one direction and prediction errors in the other). But I certainly am not trying to suggest we actually understand it all!

      2. Visual and auditory and tactile stimuli have physical properties that inhere not in the individual units (like individual photons) but in their spatial and temporal arrangement. Many aspects of that arrangement map more or less directly onto qualitative aspects of the percept (visual size, for example). With the exception of a mapping of concentration to intensity, this is not the case for chemical stimuli. The percepts are (or seem to me) much more arbitrary in nature, much less explorable, less relatable to information from the other senses. They seem to just be that way. (Whether that is universal or more idiosyncratic, they're still *some* way for any given individual).

      3. A lot of the examples you discuss in relation to experience relate to flavours, not simple taste sensations. Flavour is a much more complex thing and relies heavily on olfaction, combined with taste (and influenced by colour, sound, feel, etc). But I'm more interested here in the "perceptual primitives" of our six or seven taste categories.

    5. In response to

      1. I'm not criticizing the predictive account and I did not think you were suggesting we understand everything. I work in learning theory and while I very much like what people in radical behaviorism are doing, I agree that their learning story seems to be limited to hebbian learning, which does not capture very much. I would disagree with the inference part, but that's another discussion to have. What I was pointing out is that your conclusion to the need for a distributed, predictive system simply did not follow from your argument.

      2. The concentration you mention is still a "statistical and physical propert[y]" of the stimulus that maps to the sensation, which you had rejected for tastes and odors. The same holds for the distribution of different molecules (rather than merely the concentration of a single molecule) in a stimulus. I have a very limited understanding of chemistry, but if I'm not mistaken, then structural similarity tends to map onto functional similarity as well, so I would assume that you can predict the taste sensation from the relevant molecules' structure to some degree as well (like having that hydrogen atom). I see how spatial or temporal arrangement map onto visual perception, but I'm less clear on what the physical properties that map onto sound are. Even though it is difficult to think about taste in terms of fine-grained temporal arrangement as in the scanning of a visual scene, it makes perfect sense to me to talk about how tasting one thing influences tasting the next (like something tasting more sour after having had something sweet). And if we go back to wine, then it becomes obvious that this does not even need different stimuli, as interesting wines result in a series of sensations, rather than one that is constant.

      3. Your whole post was couched in conscious perception. Consequently, the unit of analysis needs to be that which is actually perceived. Perceptual primitives don't exist in that sense, perception is not a combinatorial process, but a discriminative one. Colour, sound and feel don't influence odour and taste, they are odour and taste, to the degree that the chemical process and the resulting nerve impulses you are talking about have not and with finite experience cannot be discriminated from the others. To quote James again, these "are all products of discrimination carried to a high pitch".

    6. Kuchenrolle said:

      >> The world does not come parsed into separate things...

      Agreed. However, the world is parsed by way of the perceptual capacities of the human nervous system.


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