Kent c. Berridge and Morten l. Kringelbach
134 II. BIOlOGIcAl perSpectIveS any pleasure in his or her life. An example of the
purely eudaimonic view of happiness was famously expressed 150 years ago by John Stuart Mill: “It is better to be a human being dissatisfied than a pig satisfied; better to be Socrates dissatisfied than a fool satisfied” (Mill, 1861/1998, p. 57). By Mill’s view as quoted here, a life filled with the most intense pleasures of pigs or fools would never be enough for happiness. Rather, true happiness was presumed by that view to hinge on a superior kind of richness of life meaning and engagement that was possessed fully by the enlightened Socrates, even when facing a death sentence, no matter how much hedonically dissatisfied he might have been.
Yet even Mill (1861/1998) himself seemed to imply elsewhere that hedonic pleasure was im- portant to happiness too. And conversely, other psychologists have emphasized the hedonic side of happiness, sometimes at the expense of eudai- monia. For example, Sigmund Freud (1930) ap- peared nearly to take a purely hedonic view of hap- piness in his book Civilization and Its Discontents.
Freud wrote there, in response to his own question
“What do people ask of life and wish to achieve in it?” his personal reply:
The answer to this can hardly be in doubt. They strive after happiness; they want to become happy and to remain so. This endeavor has two sides, a positive and a negative aim. It aims, on the one hand, at an absence of pain and displeasure, and, on the other, at the experiencing of strong feelings of plea- sure. (p. 76)
Freud’s answer essentially equates pleasure with happiness. According to this view, the more plea- sure you have (while avoiding displeasure), the happier you will be.
It may not be necessary to choose either hedo- nia or eudaimonia over the other. Most modern psychologists who study happiness tend to fall in between the poles illustrated by Mill and Freud, and hold hedonic factors to be crucially important to well-being (Kahneman, Diener, & Schwarz, 1999; Gilbert, 2006; Kahneman, Krueger, Schkade, Schwarz, & Stone, 2006; Biswas-Diener, Kashdan, & King, 2009; Diener, 2012; Jayawick- reme, Forgeard, & Seligman, 2012), even when es- pousing views that on the whole emphasize eudai- monic factors (Peterson & Park, 2009; Seligman, Railton, Baumeister, & Sripada, 2013). We simi- larly presume that a capacity for taking pleasure in life is an important feature of happiness, but do not reduce happiness to pleasure nor ignore the importance of eudaimonic aspects of well-being.
However, our main point is simply that if happi- ness involves a pleasurable or hedonic component, then finding brain mechanisms for pleasure may give insight into the hedonic aspects of well-being.
A better understanding of the hedonic component of happiness in turn might be used as a first step toward understanding the brain mechanisms of happiness more generally, given that both aspects tend to cluster together in happy individuals. It is important to note that our focus on the hedonia component of happiness should not be confused with hedonism, which is the pursuit of pleasure for pleasure’s own sake, and more akin to the ad- diction features we describe below. Also, to focus on hedonics does not deny that some ascetics may have found bliss through painful self-sacrifice, but simply reflects that positive hedonic tone is indis- pensable to most people seeking happiness.
Most important to our suggestion that it is not necessary to choose between hedonia and eudai- monia is the empirical finding that a high corre- lation actually exists between the pleasurable and the life-meaning aspects of happiness when rated by individuals—that is, the same lucky individu- als who tend to score highest on a eudaimonic measure of happiness also tend to score highest on their hedonic ratings of happiness (Diener, Ke- sebir, & Lucas, 2008; Kuppens, Realo, & Diener, 2008). Those who have one also have the other.
Conversely, individuals who are lowest on a he- donic measure tend to also be lowest on the eudai- monic measure. Fortunately, it turns out that most people report themselves to be reasonably happy.
For example, in happiness surveys, over 80% of people rate their overall eudaimonic life satisfac- tion as “pretty to very happy,” and 80% also rate their current hedonic mood as positive (e.g., posi- tive = 6–7 on a 10–point valence scale, where 5 is “hedonically neutral”; Diener et al., 2008; Kup- pens et al., 2008). A lucky happy few may even live consistently around a hedonic point of 8.
In our view, this tendency of pleasure ratings and meaningfulness ratings to correlate together opens a potential window of opportunity to af- fective neuroscience in understanding the brain bases of happiness. Hedonic well-being in particu- lar, which can be studied relatively easily, presents a practical gateway to the more difficult-to-study state of eudaimonic well-being (Urry, et al., 2004;
Kringelbach & Berridge, 2009). In other words, if both hedonia and eudaimonia co-occur in the same happy people, then identifying neural mark- ers of hedonia may offer a toehold into identifying neural bases of eudaimonia. In this way, studies of
7. From pleasure to Happiness 135 hedonic well-being, which tend to be more amena-
ble to neuroscience approaches than eudaimonic meaningfulness of life, may help to identify brain markers that distinguish happy people, including at least some brain markers that will turn out to overlap with eudaimonic well-being.
Many Different Pleasures but One Brain Pleasure System?
Subjectively, the sensory pleasure of a delicious- tasting food feels very different from the sensory pleasures of sex or of drugs. And subjectively there is even more difference between such sensory plea- sures and any higher social or cognitive pleasures, such as seeing a loved one or listening to music. Yet affective neuroscience evidence has emerged in the past decade to suggest that brain mechanisms of sensory pleasures overlap to a surprising degree with brain mechanisms of cognitive, cultural, and social pleasures, and even with mechanisms of hedonic well-being. Evidence from neuroimag- ing studies suggests there is a single shared core process of positive affect shared by many diverse hedonic experiences and positive emotions, even those that may each subjectively feel quite differ- ent and unique (Rozin, Haidt, & Fincher, 2009;
Kringelbach & Berridge, 2010b; Lindquist, Wager, Bliss-Moreau, Kober, & Barrett, 2012; Wilson- Mendenhall, Barrett, & Barsalou, 2013). The list of brain structures activated by all these pleasures includes several limbic regions within the prefron- tal cortex: for example, the orbitofrontal, anterior cingulate, and insula cortices. Brain structures activated by diverse pleasures also include several subcortical limbic structures, such as the nucleus accumbens (NAc), ventral pallidum, amygdala, and mesolimbic tegmentum (which contains do- pamine neurons; Beauregard & Paquette, 2006;
Harris et al., 2009; Frijda, 2010; Leknes & Tracey, 2010; Skov, 2010; Vuust & Kringelbach, 2010;
Salimpoor, Benovoy, Larcher, Dagher, & Zatorre, 2011; Lindquist, Wager, Kober, Bliss-Moreau, &
Barrett, 2012; Wilson-Mendenhall et al., 2013).
The range of pleasures that activate such over- lapping brain structures spans from mere sensory pleasures of food, sex, or addictive drugs to human cognitive, social, and even moral pleasures such as the encounter of favorite music, art, a loved one, or religious ecstasy.
The strong degree of neural overlap in hedonic circuitry gives rise to the hypothesis that there is a shared underlying “neural currency” or mesocorti-
colimbic mechanism for generating the pleasure of all those psychologically diverse experiences and emotions (Kringelbach & Berridge, 2010b). Evolu- tionarily, this could be understood by saying that the brain seems to have conserved the mecha- nisms that evolved originally to generate sensory pleasures, and extended their pleasure functions to higher pleasures that appeared later in human evo- lution. Rather than having to invent entirely new brain systems for generating abstract social or cog- nitive pleasures, the human brain seems to have simply adapted original sensory pleasure mecha- nisms, and integrated them with new cognitive inputs, to produce the higher human pleasures.
This overlap or common neural currency idea implies that what can be learned about the de- tails of how the brain generates one pleasure may also apply to many other forms of pleasure. Most of what affective neuroscience has learned so far about pleasure in the brain has come from studies of sensory pleasures, such as food pleasures or drug pleasures. But based on the common neural cur- rency idea, we suggest that what has been learned about how those sensory pleasures are produced by brain systems may also provide insights into how the same brain systems produce higher pleasures.
So for example, conclusions described below about how sensory pleasure is coded by the orbitofrontal cortex or generated by limbic hedonic hot spots may similarly apply the coding and generation of cognitive and social pleasures too. This extension of shared hedonic mechanisms is useful at least as a hypothesis for guiding future studies of higher pleasures.
Of course, it is possible that future studies with improved technology will find subtle differences in neurobiological operation or tiny patterns of subregional anatomical localization within a par- ticular brain structure that may help distinguish different types of pleasures. But alternatively, the reason why they feel so different may have to do with other nonhedonic sensory and cognitive aspects of the pleasurable experiences, which are mediated by other brain structures, rather than hedonic differences in the pleasures themselves.
The common neural currency idea may extend even to the sustained and free-floating pleasant state of happiness itself. Some direct evidence for this idea comes from an intriguing study by Heller and colleagues (2013), which reported that high subjective ratings in response to questions such as “In general, [do] I feel confident and positive about myself?” were correlated with high sustained functional magnetic resonance imaging (fMRI)
136 II. BIOlOGIcAl perSpectIveS measures of brain activation in the subcortical nu-
cleus accumbens (ventral striatum). The nucleus accumbens is a major target of the brain’s meso- limbic dopamine “wanting” system for reward, and also contains an opioid hedonic hot spot for generating the intense “liking” of a sensory plea- sure, as discussed below. Thus there appears to be substantial overlap between brain mechanisms of abstract human pleasures, including hedonic happiness, with the older mechanisms of specific sensory pleasures, shared with animals, which we describe next.
Sensory Pleasures: From Sensation to “Liking” to hedonic Feelings
What makes a pleasure so nice? Pleasure or posi- tive affect is never merely a sensation, not even for a sensory pleasure such as sweetness (Ryle, 1954;
Frijda, 2010; Kringelbach, 2010; Kringelbach &
Berridge, 2010b). Instead, the hedonic quality al- ways requires the recruitment of specialized plea- sure-generating brain systems to actively paint an additional “hedonic gloss” onto a sensation. Ac- tive recruitment of brain pleasure-generating sys- tems is what makes a pleasant experience liked.
These pleasure-generating systems have been shown by recent studies to take the form of a network of small “hedonic hot spots” distributed at several layers throughout the brain. Together, those hedonic hot spots interact together to make a sensation become positively liked.
Pleasure is always added to stimuli actively by the brain to make them positively hedonic, and is not an immutable feature of any external stimu- lus or event itself. The capacity of certain stimuli, such as a sweet taste or a loved one, to reliably elicit pleasure—to nearly always be painted with a hedonic gloss—reflects their privileged ability to activate those hedonic brain systems responsible for manufacturing and applying the gloss.
Hedonic brain systems involving multiple cod- ing sites and generating hot spots are well devel- oped in the brain, spanning subcortical and cor- tical levels. The basic circuitry wiring pattern is quite similar across humans and other animals (Heimer, Van Hoesen, Trimble, & Zahm, 2008).
Why hedonic brain networks are so robust, and why they are relatively similar across humans and other animals, is probably because hedonic reac- tions have long had adaptive function. The basic hedonic circuits of the brain were formed and selected rather early in mammalian evolution. It
seems unlikely so much neural machinery would have been preserved across evolutionary time if it had no function. Basic pleasure reactions have always had objective consequences, and brain mechanisms for hedonic reactions have long been functionally useful—even before any additional mechanisms appeared that characterize any hu- man-unique aspects of subjective feelings of plea- sure. In a sense, hedonic reactions have been too important to survival for pleasure to be exclusively in the realm of subjective experience.
Pleasure as an adaptive evolutionary feature is not so hard to imagine. For example, tasty food is one of the most universal routes to pleasure, as well as an essential requirement to survival. Not accidentally, food is also one of the most accessible experimental methods available to psychology and neuroscience studies of pleasure (Rozin, 1999;
Kringelbach, 2005; Peciña, Smith, & Berridge, 2005; Berridge, Ho, Richard, & DiFeliceantonio, 2010; Gottfried, 2010; Kringelbach & Berridge, 2010a; Veldhuizen, Rudenga, & Small, 2010).
Much of what is currently known about pleasure in the brain comes from such studies, including which cortical sites most faithfully code pleasure and which brain sites are hedonic hot spots to help generate pleasure.
Identifying Pleasure Generators in the Brain
Pleasant experiences such as a sensory pleasure or a positive emotion may appear in experience to be a unitary process, but virtually all are complex composites of affective and cognitive processes (Russell & Barrett, 1999; Clore & Ortony, 2000;
Lambie & Marcel, 2002; Ellsworth & Scherer, 2003; Lindquist, Wager, Bliss-Moreau, et al., 2012;
Chapter 15, this volume). Affective neuroscience studies have further indicated that even the sim- plest pleasant experience, such as a mere sensory reward, is actually a more complex set of processes containing several psychological components, each with distinguishable neurobiological mecha- nisms (Berridge, Robinson, & Aldridge, 2009;
Kringelbach & Berridge, 2009; Leknes & Tracey, 2010). These include, in particular, distinct com- ponents of reward wanting versus reward liking (as well as reward learning), and each psychological component has both conscious and nonconscious subcomponents. Liking is the actual pleasure com- ponent or hedonic impact of a reward; wanting is the motivation for reward; and learning includes
7. From pleasure to Happiness 137 the associations, representations, and predictions
about future rewards based on past experiences.
Each of these components has brain mechanisms that are different from mechanisms of the other components, and each plays a central role in the cyclical time course of a pleasant experience (Plates 7.1 and 7.2; see color insert for plates).
The conscious experience of pleasure is so strik- ing that pleasure has seemed purely subjective by definition to many thinkers. But related to the no- tion that pleasure naturally evolved, we think that pleasure also has objective aspects that can be de- tected in brain and behavior. This is related to the underlying similarities of brain limbic mechanisms for generating sensory pleasures across the brains of most mammals, both humans and nonhumans alike. The objective aspect has been invaluable in identifying the brain generators of pleasure de- scribed below.
We distinguish between the conscious and nonconscious aspects of these subcomponents be- cause both exist in people (Winkielman, Berridge,
& Wilbarger, 2005). And at least the latter can also be studied in other animals in ways that help reveal the underlying neural-generating mecha- nisms. At the potentially nonconscious level, we use quotation marks to indicate that we are de- scribing objective, behavioral, or neural measures of these underlying brain processes. As such, “lik- ing” reactions result from activity in identifiable brain systems that paint hedonic value on a sen- sation such as sweetness, and produce observable affective reactions in the brain and in behavior such as facial expressions. Similarly, “wanting” in- cludes incentive salience or motivational processes within reward that mirror hedonic “liking” and make stimuli into motivationally attractive incen- tives. “Wanting” helps spur and guide motivated behavior, when incentive salience is attributed to stimulus representations by the mesolimbic brain systems. Finally, “learning” includes a wide range of processes linked to implicit knowledge as well as associative conditioning, such as basic Pavlovian and instrumental associations.
At the conscious level, “liking” is the subjec- tive feeling of pleasure in the ordinary sense of the word, which may be elaborated out of (mostly subcortical) core liking reactions by cognitive brain mechanisms of awareness. Conscious want- ing includes conscious desires for incentives or cognitive goals, while conscious learning includes the updating of explicit and cognitive predictions (Friston & Kiebel, 2009; Zhang, Berridge, Tindell, Smith, & Aldridge, 2009).
By themselves, core “liking” and “wanting” pro- cesses can occur nonconsciously, even in normal people. For example, viewing a subliminally brief happy facial expression or angry facial expres- sion for just one-sixtieth of a second produces no change in people’s conscious emotional feelings, and they remain unaware of having seen the emo- tional expressions. They are unable to pick the photo they saw out of a lineup (especially if the subliminal emotional expression is followed by a longer view of a neutral face, and if the experience is embedded in a task that distracts the viewers because they are concentrated on performing it correctly). Yet subliminal exposures to the happy face can make the viewers subsequently go on to evaluate a new stimulus (e.g., a flavored drink pre- sented as a new marketing product) much more positively and to consume more of that stimulus, whereas exposure to the angry face makes view- ers evaluate the new stimulus more negatively and consume less of it, indicating that the subliminal emotional expressions had induced nonconscious
“liking” versus “disliking” reactions that never surfaced into conscious emotional feelings but remained able to alter their behavior under par- ticular circumstances (Berridge & Winkielman, 2003). Such observations of nonconscious hedonic reactions suggests that additional brain circuitry is needed to convert a core “liking” reaction into a consciously liked experience of felt pleasure. Of course, it remains a major mystery precisely which brain circuits or neural operations are responsible for generating consciousness, including conscious experiences of subjective pleasure or of subjective feelings of desire. Traditional answers have tended to favor neocortex, and especially perhaps the pre- frontal lobe of the cortex. The prefrontal cortex is quite prominent in humans, and includes several limbic regions such as the orbitofrontal cortex, an- terior cingulate cortex, and insula (deep in the lat- eral surface of the prefrontal cortex, buried under the temporal lobe). However, this consciousness assignment to the prefrontal cortex may have more to do with tradition, and with the traditional assumption that what appears anatomically well developed in humans must necessarily have to do with human consciousness, than with any particu- lar evidence.
Indeed, to the contrary, what evidence is avail- able suggests that conscious feelings of liking, wanting, or other emotions can persist surprisingly well even in humans in essentially the complete absence of the prefrontal cortex. For example, a re- cent study reported remarkably normal emotion in