Sunday, 20 July 2014

A taste of emotion

If you study perception, you tend not to be particularly concerned with the “secondary” emotions that sensory experiences might evoke (for a fuller discussion of this, see: http://www.expo.rai.it/eng/2014/07/08/taste-neuroscience-prescott/). Except if you study taste, in which case you can hardly avoid it. Emotional responses to tastes are, we can say with a reasonable degree of certainty, built into the fabric of the taste experience. Jacob Steiner’s famous photographs of newborns smiling or grimacing in response to sucrose and quinine [1], respectively, are if not exactly proof of this, then nevertheless compelling. The adaptive argument, too, is simple: tastes evoke emotions because this activates motivations to consume (calories, salt) or avoid (toxins) and hence promote survival. 

Our everyday language provides us with some hints that taste may find links with our emotions more broadly. Thus, unpleasant emotional experiences will leave a bitter taste in your mouth; we say that we can taste the fear, and of course sweetness is synonymous with all sorts of pleasant emotions.  The usual interpretation of such figures of speech is that we have co-opted tastes to help us describe emotions, perhaps because we tend to be poor at this.

But increasingly this does not seem to be the whole picture. A recently published study by Herbert and colleagues [2] examined the way in which autonomic nervous system responses - eye-blinks and changes in pupil diameter in response to startling bursts of white noise - are modified by emotion-inducing pictures. Importantly, though, they compared these responses in tasters and non-tasters of the bitter compound 6-n-propylthiouracil (PROP). This study was prompted by an earlier study in which PROP supertasters showed more intense self-reported emotional responses (anger, tension, sadness and fear; decreased mood and joy) than non-tasters or medium tasters after an anger-inducing film clip.

Herbert and colleagues found that startle responses were increased for pictures meant to elicit fear, anger, disgust, or pictures that were pleasant in content, relative to neutral pictures – but in the PROP-taster group only, and not the non-tasters. This suggests that the PROP tasters are hyper-responsive to both negative and positive emotions generally, not just to tastes.

Why would broad emotional responsiveness be linked to the ability to taste a particular bitter compound? Certainly, facial expressions to bitterness – the familiar grimace, nose-wrinkle and gape – has previously been thought to be the basis of the classic disgust facial response and perhaps even the origin of this basic emotion itself. Indeed, PROP super-tasters has been shown to be more responsive to the visceral – but not moral – aspects of disgust than are (medium) tasters and non-tasters, with taste sensitivity being positively correlated with degree of disgust [3].

But a common origin for disgust and bitterness dislike suggests something broader than the involvement of one particular bitter compound linked to a specific taste receptor (T2R38), one of perhaps 30 or more such bitter receptors. Two possibilities suggest themselves. The first is that responses to bitterness in general are reflective of an underlying overall emotional responsiveness, a relationship yet to be tested. In this sense, bitter substances are simply effective at eliciting emotions, in the same way as pictures of disgusting scenes or objects are effective. In addition, though, ratings of PROP intensity are often used as a proxy measure for taste responsiveness in general. PROP tasters also find sweet, salty sour and bitter tastes more intense than do PROP non-tasters (see for example, [4]).  This is more than likely due to the fact that increased numbers of taste buds underlie overall taste responsiveness, including (at least for those not ‘blind’ to it), PROP bitterness.

It has been hypothesized for some time that the pleasure given by sweetness is really no different than pleasure of any other sort, and that a common reward system in the brain underlies the popularity of sex, drugs and rock ‘n roll ….. and cake. But yet another broad link between taste and more general responsiveness to reward has been reported [5]. I have discussed the phenomenon of sweet liking and disliking previously (How sweet it is ... or is it?). The origins of this hedonic dimension are not well understood, but this study suggests that it may be linked to variations in overall disinhibition. Here, disinhibition was defined in terms of delay discounting – the idea of how much we value a given reward given now versus one that may be much larger, if we are willing to wait for it. So, if I say that I would rather have $10 now rather than $20 in a month, I am effectively discounting the later amount. In food terms, I can have one piece of chocolate now or three pieces in an hour. If you opt for the smaller reward now, you are unable to inhibit your need to satisfy your immediate desire. It turns out that such “discounters” are more likely to be sweet likers, that is, to prefer higher levels of sweetness. This then is another case of taste responses being seen in terms of more general responsiveness to reward.

An obvious interpretation is that, as mentioned above, pleasant tastes are merely part of an overall reward system that has adaptive value. However, there is an intriguing alternative explanation of why tastes might be so tied into other aspects of emotional life. If we start with the premise that tastes are responsible for some of the earliest emotions that we experience, it becomes possible to think about these early experiences having a large impact in shaping our broader emotional landscape. So, in this scenario, the fact you respond more positively to sweetness than I do becomes a major factor in whether or not you delay discount, not just for chocolates but in general for all reward. Similarly, sensitivity to bitterness – present at birth – has such a strong emotional impact that it influences the way you subsequently respond to all emotional stimuli. As a corollary, individual variations in taste sensitivity or hedonic value becomes a primary determinant of variations in our emotional responsiveness generally. 

Admittedly, this is a “chicken/egg” argument that may be impossible to determine but ….. the chronological primacy of taste hedonics does mean that we ought to consider the possibility that the taste of fear is not a way of helping us describe emotions but rather a clue to where our emotions originate.
____________________________________________________________________

1. Steiner, J.E., et al., Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. . Neurosci. Biobehav. Rev., 2001. 25(1): p. 53-74.
2. Herbert, C., et al., Supertaster, super reactive: Oral sensitivity for bitter taste modulates emotional approach and avoidance behavior in the affective startle paradigm. Physiol Behav, 2014. 135C: p. 198-207.
3. Herz, R.S., PROP Taste Sensitivity is Related to Visceral but Not Moral Disgust. Chem. Percept., 2011. 4: p. 72-79.
4. Prescott, J., N. Ripandelli, and I. Wakeling, Intensity of tastes in binary mixtures in PROP non-tasters, medium-tasters and super-tasters. . Chem. Senses, 2001. 26: p. 993-1003.
5.    Weafer, J., A. Burkhardt, and H. de Wit, Sweet taste liking is associated with impulsive behaviors in humans. Front Behav Neurosci, 2014. 8: p. 228.