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Pleasure Systems in the Brain

2015; Cell Press; Volume: 86; Issue: 3 Linguagem: Inglês

10.1016/j.neuron.2015.02.018

1097-4199

Kent Berridge, Morten L. Kringelbach,

Sleep and Wakefulness Research

Pleasure is mediated by well-developed mesocorticolimbic circuitry and serves adaptive functions. In affective disorders, anhedonia (lack of pleasure) or dysphoria (negative affect) can result from breakdowns of that hedonic system. Human neuroimaging studies indicate that surprisingly similar circuitry is activated by quite diverse pleasures, suggesting a common neural currency shared by all. Wanting for reward is generated by a large and distributed brain system. Liking, or pleasure itself, is generated by a smaller set of hedonic hot spots within limbic circuitry. Those hot spots also can be embedded in broader anatomical patterns of valence organization, such as in a keyboard pattern of nucleus accumbens generators for desire versus dread. In contrast, some of the best known textbook candidates for pleasure generators, including classic pleasure electrodes and the mesolimbic dopamine system, may not generate pleasure after all. These emerging insights into brain pleasure mechanisms may eventually facilitate better treatments for affective disorders. Pleasure is mediated by well-developed mesocorticolimbic circuitry and serves adaptive functions. In affective disorders, anhedonia (lack of pleasure) or dysphoria (negative affect) can result from breakdowns of that hedonic system. Human neuroimaging studies indicate that surprisingly similar circuitry is activated by quite diverse pleasures, suggesting a common neural currency shared by all. Wanting for reward is generated by a large and distributed brain system. Liking, or pleasure itself, is generated by a smaller set of hedonic hot spots within limbic circuitry. Those hot spots also can be embedded in broader anatomical patterns of valence organization, such as in a keyboard pattern of nucleus accumbens generators for desire versus dread. In contrast, some of the best known textbook candidates for pleasure generators, including classic pleasure electrodes and the mesolimbic dopamine system, may not generate pleasure after all. These emerging insights into brain pleasure mechanisms may eventually facilitate better treatments for affective disorders. The English word “hedonic” comes originally from the ancient Greek for pleasure (η´δovη´; in Latin script: hédoné), in turn derived from the word for “sweet” (η´δv´ς or hēdús). Today hedonic refers to sensory pleasures as well as many higher types of pleasure (e.g., cognitive, social, aesthetic, and moral). Some goals of affective neuroscience are to understand how brain mechanisms generate pleasures, and also displeasures, and eventually find more effective treatments for affective disorders (Anderson and Adolphs, 2014Anderson D.J. Adolphs R. 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The basic emotional circuits of mammalian brains: do animals have affective lives?.Neurosci. Biobehav. Rev. 2011; 35: 1791-1804Crossref PubMed Scopus (0) Google Scholar). Capacity for normal pleasure is essential to healthy psychological function or well-being. Conversely, affective disorders can induce either the pathological absence of pleasure reactions (as in clinical anhedonia) or the presence of excessive displeasure (dysphoric emotions such as pain, disgust, depression, anxiety, or fear). But is a neuroscience of pleasure feasible? Doubts that pleasure might be scientifically understood have been expressed for over a century. Early doubts stemmed from behaviorist convictions that only objective behavioral-neural reactions were eligible for scientific study and never subjective experiences (including the experience of pleasure). However, progress in the past 50 years proves that many complex psychological processes involving subjective experience can be successfully studied and related to underlying brain mechanisms. Still, some objections persist today. For example, LeDoux’s recent recommendation that affective neuroscientists should focus only on behavioral affective reactions, rather than on subjective emotions, shares those earlier concerns (LeDoux, 2014LeDoux J.E. Coming to terms with fear.Proc. Natl. Acad. Sci. USA. 2014; 111: 2871-2878Crossref PubMed Scopus (0) Google Scholar). In our view, a neuroscience of pleasure can be pursued as successfully as the neuroscience of perception, learning, cognition, or other well-studied psychological functions. The crucial test of this proposition is: can affective neuroscience produce important new conclusions into how brain systems mediate hedonic impact? Evidence in support of this, we think, now exists in the form of recent findings. In this article we discuss some of these new findings, including (1) separation of reward liking, wanting, and learning mechanisms in mesocorticolimbic circuitry; (2) identification of overlap in neural circuitry underlying sensory pleasures and higher pleasures; (3) identification of particular sites in prefrontal limbic cortex that encode pleasure impact; (4) mapping of surprisingly localized causal hedonic hot spots that generate amplifications of pleasure reactions; (5) discovery that nucleus accumbens (NAc) hot spot and cold spot mechanisms are embedded in an anatomically tuned keyboard organization of generators in NAc that extends beyond reward liking and wanting to negative emotions of fear and disgust; and (6) identification of multiple neurochemical modes within NAc mechanisms that can retune keyboard generators into flipping between oppositely valenced motivations of desire and dread. In a sense, pleasure can be thought of as evolution’s boldest trick, serving to motivate an individual to pursue rewards necessary for fitness, yet in modern environments of abundance, also inducing maladaptive pursuits such as addictions. An important starting point for understanding the underlying circuitry is to recognize that reward involves a composite of several psychological components: liking (core reactions to hedonic impact), wanting (motivation process of incentive salience), and learning (Pavlovian or instrumental associations and cognitive representations) (Berridge and Robinson, 2003Berridge K.C. Robinson T.E. Parsing reward.Trends Neurosci. 2003; 26: 507-513Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar). These component processes also have discriminable neural mechanisms. The three processes can occur together at any time during the reward-behavior cycle, though wanting processes tend to dominate the initial appetitive phase, while liking processes dominate the subsequent consummatory phase that may lead to satiety. Learning, on the other hand, happens throughout the cycle. A neuroscience of reward seeks to map these components onto necessary and sufficient brain networks (see Figure 1). To study pleasure comprehensively, good human neuroimaging studies are needed to explore correlative encoding of pleasant experiences and good animal studies are needed to explore causation of underlying hedonic reactions. This two-pronged approach exploits a fundamental duality in hedonic processes, related to the objective versus subjective faces of pleasure (Damasio and Carvalho, 2013Damasio A. Carvalho G.B. The nature of feelings: evolutionary and neurobiological origins.Nat. Rev. Neurosci. 2013; 14: 143-152Crossref PubMed Scopus (0) Google Scholar, Kringelbach and Berridge, 2010Kringelbach M.L. Berridge K.C. Pleasures of the Brain. Oxford University Press, Oxford2010Google Scholar, Schooler and Mauss, 2010Schooler J.W. Mauss I.B. To be happy and to know it: The experience and meta-awareness of pleasure.in: Kringelbach M.L. Berridge K.C. Pleasures of the Brain. Oxford University Press, Oxford, U.K.2010: 244-254Google Scholar, Winkielman et al., 2005Winkielman P. Berridge K.C. Wilbarger J.L. Unconscious affective reactions to masked happy versus angry faces influence consumption behavior and judgments of value.Pers. Soc. Psychol. Bull. 2005; 31: 121-135Crossref PubMed Scopus (0) Google Scholar). Pleasure is sometimes assumed to be a purely subjective feeling. But pleasure also has objective features in the form of measurable hedonic reactions, both neural and behavioral, to valenced events. In this review, we denote objective hedonic reactions as “liking” reactions (with quotes) to distinguish them from the subjective experience of liking (in the ordinary sense, without quotes). Objective hedonic reactions can be measured in both human and animal neuroscience studies, which together allow some comparisons across species and can lead to a more complete causal picture of how brain systems mediate hedonic impact. The ultimate explanation for why pleasure encompasses both objective and subjective levels of reaction likely lies in evolutionary history. Darwin, 1872Darwin C. The Expression of the Emotions in Man and Animals, (1998 edition: revised and with commentary by P. Ekman). Harper Collins - Oxford University Press, Oxford1872Crossref Google Scholar originally suggested that affective reactions were selected by evolution for their useful functions, which were adapted into emotional expressions. Following Darwin’s logic, modern affective neuroscience also posits brain mechanisms of emotional reactions to mediate evolved “survival functions” (LeDoux, 2012LeDoux J. Rethinking the emotional brain.Neuron. 2012; 73: 653-676Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar), with emotional “core features that can form the basis for studies of emotion across phylogeny” (p. 198) (Anderson and Adolphs, 2014Anderson D.J. Adolphs R. A framework for studying emotions across species.Cell. 2014; 157: 187-200Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar), which can be usefully exploited by objective studies. The selection of hedonic reactions has required the evolution of mammalian brains to dedicate millions of developing neurons into mesocorticolimbic patterns of reward circuitry (Haber and Knutson, 2010Haber S.N. Knutson B. The reward circuit: linking primate anatomy and human imaging.Neuropsychopharmacology. 2010; 35: 4-26Crossref PubMed Scopus (1031) Google Scholar). Such neural investment was subject to the same selection pressures that shaped evolution of any other function. Hedonic circuitry was therefore unlikely to have been shaped into its present form, or to have persisted throughout evolution, unless objective affective reactions actually conveyed significant consequences in terms of benefits for survival and fitness (Anderson and Adolphs, 2014Anderson D.J. Adolphs R. A framework for studying emotions across species.Cell. 2014; 157: 187-200Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar, Damasio, 2010Damasio A.R. Self Comes to Mind: Constructing the Conscious Brain.First Edition. Pantheon Books, New York2010Google Scholar, Kringelbach and Berridge, 2010Kringelbach M.L. Berridge K.C. Pleasures of the Brain. Oxford University Press, Oxford2010Google Scholar, LeDoux, 2012LeDoux J. Rethinking the emotional brain.Neuron. 2012; 73: 653-676Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar, Panksepp, 2011Panksepp J. The basic emotional circuits of mammalian brains: do animals have affective lives?.Neurosci. Biobehav. Rev. 2011; 35: 1791-1804Crossref PubMed Scopus (0) Google Scholar). Objective affective reactions likely appeared first during evolution, with subjective affective reactions following in some species, via the evolution of more elaborate and hierarchical brain mesocorticolimbic circuitry to translate core “liking” reactions into conscious feelings of pleasure (Damasio and Carvalho, 2013Damasio A. Carvalho G.B. The nature of feelings: evolutionary and neurobiological origins.Nat. Rev. Neurosci. 2013; 14: 143-152Crossref PubMed Scopus (0) Google Scholar). A useful example of an objective hedonic reaction is the orofacial affective expression of “liking” elicited by tastes in newborn human infants (Steiner, 1973Steiner J.E. The gustofacial response: observation on normal and anencephalic newborn infants.Symp. Oral Sens. Percept. 1973; 4: 254-278PubMed Google Scholar). Positive taste “liking” versus negative “disgust” expressions can be elicited on the first post-natal day (Figure 1). Sweet tastes elicit positive hedonic “liking” expressions comprising relaxed facial muscles and a contented licking of the lips, whereas bitter tastes elicit “disgust” expressions. Homologous “liking” orofacial expressions can be elicited also in apes and monkeys and even in rats and mice (e.g., rhythmic tongue protrusions and lateral lip licking to sweetness versus gapes and headshakes to bitterness) (Berridge, 2000Berridge K.C. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns.Neurosci. Biobehav. 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Percept. 1973; 4: 254-278PubMed Google Scholar), but such affective expressions are not mere brainstem reflexes, but rather are hierarchically controlled by forebrain structures. Forebrain circuitry exerts powerful descending control over brainstem and behavioral output. A consequence is that “liking” expressions elicited by a given taste are appropriately modulated physiologically by relevant appetite versus satiety states (Cabanac and Lafrance, 1990Cabanac M. Lafrance L. Postingestive alliesthesia: the rat tells the same story.Physiol. Behav. 1990; 47: 539-543Crossref PubMed Scopus (0) Google Scholar, Kaplan et al., 2000Kaplan J.M. Roitman M. Grill H.J. Food deprivation does not potentiate glucose taste reactivity responses of chronic decerebrate rats.Brain Res. 2000; 870: 102-108Crossref PubMed Scopus (0) Google Scholar), as well as associatively by learned preferences and aversions (Delamater et al., 1986Delamater A.R. LoLordo V.M. Berridge K.C. Control of fluid palatability by exteroceptive Pavlovian signals.J. Exp. Psychol. Anim. Behav. Process. 1986; 12: 143-152Crossref PubMed Scopus (0) Google Scholar). Most strikingly, “liking” reactions are powerfully controlled by discrete neural manipulations located in several limbic forebrain structures, as will be discussed (Castro and Berridge, 2014Castro D.C. Berridge K.C. Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting”.J. Neurosci. 2014; 34: 4239-4250Crossref PubMed Scopus (51) Google Scholar, Mahler et al., 2007Mahler S.V. Smith K.S. Berridge K.C. Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances ‘liking’ of a sweet reward.Neuropsychopharmacology. 2007; 32: 2267-2278Crossref PubMed Scopus (0) Google Scholar, Peciña and Berridge, 2005Peciña S. Berridge K.C. 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Those hedonic reactions co-occur with several other ingestive consummatory reactions, including voluntary consumption of food, the microstructure of consumption movements (often measured as spout-lick patterns by lickometers in animal studies), and the simple brainstem decision to swallow food in the mouth. But consummatory reactions are highly heterogeneous. In particular, affective taste reactivity patterns most closely track the hedonic evaluation of taste “liking” and sometimes for that reason dissociate from all other consummatory reactions (Berridge, 2000Berridge K.C. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns.Neurosci. Biobehav. Rev. 2000; 24: 173-198Crossref PubMed Scopus (356) Google Scholar). Dissociation is most commonly induced by manipulations that alter motivational (i.e., “wanting”), but not hedonic aspects (“liking”) of the value of a food incentive. For example, dopamine suppressions reduce the incentive value of sweetness similar to sucrose dilution, as reflected in changes in lickometer measures of ingestive microstructure (Galistu and D’Aquila, 2012Galistu A. D’Aquila P.S. Effect of the dopamine D1-like receptor antagonist SCH 23390 on the microstructure of ingestive behaviour in water-deprived rats licking for water and NaCl solutions.Physiol. Behav. 2012; 105: 230-233Crossref PubMed Scopus (0) Google Scholar, Smith, 1995Smith G.P. Dopamine and food reward.in: Morrison A.M. Fluharty S.J. Psychobiology and Physiological Psychology. Academic Press, New York1995: 83-144Google Scholar), as well as suppressing appetitive seeking and sometimes food intake (Wise and Raptis, 1986Wise R.A. Raptis L. Effects of naloxone and pimozide on initiation and maintenance measures of free feeding.Brain Res. 1986; 368: 62-68Crossref PubMed Google Scholar). Yet, taste reactivity “liking” expressions are not diminished by such pharmacological dopamine blockades (Peciña et al., 1997Peciña S. Berridge K.C. Parker L.A. Pimozide does not shift palatability: separation of anhedonia from sensorimotor suppression by taste reactivity.Pharmacol. Biochem. Behav. 1997; 58: 801-811Crossref PubMed Scopus (0) Google Scholar), or even by complete destruction of mesolimbic dopamine projections. Such dissociations have indicated that dopamine is not actually needed for the hedonic impact of food pleasure, but rather only for their incentive motivation value, as described further below. As mentioned above, to avoid confusion it is useful to use “liking” (in quotes) to specifically refer to behavioral or neural hedonic reactions, whether or not those objective “liking” reactions are accompanied by a corresponding conscious liking or feeling of pleasure (which may require additional neural mechanisms). A similar distinction applies to conscious wanting versus the mesolimbic motivation process of incentive salience or “wanting” and its objective consequences. The subjective versus objective distinction is based also on evidence that, even in humans, the two forms of hedonic reaction can be independently measured. For example, objective hedonic “liking” reactions can sometimes occur alone and unconsciously in ordinary people without any subjective pleasure feeling at all, at least in particular situations (e.g., evoked by subliminally brief or mild affective stimuli) (Childress et al., 2008Childress A. Ehrman R. Wang Z. Li Y. Sciortino N. Hakun J. Jens W. Suh J. Listerud J. Marquez K. et al.Prelude to passion: limbic activation by “unseen” drug and sexual cues.PLoS ONE. 2008; 3: e1506Crossref PubMed Scopus (0) Google Scholar, Fischman and Foltin, 1992Fischman M.W. Foltin R.W. Self-administration of cocaine by humans: a laboratory perspective.in: Bock G.R. Whelan J. 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However, dissociations between the two levels of hedonic reaction can still sometimes occur in normal people due to the susceptibility of subjective ratings of liking to cognitive distortions by framing effects, or as a consequence of theories concocted by people to explain how they think they should feel (Gilbert and Wilson, 2009Gilbert D.T. Wilson T.D. Why the brain talks to itself: sources of error in emotional prediction.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009; 364: 1335-1341Crossref PubMed Scopus (0) Google Scholar, Schooler and Mauss, 2010Schooler J.W. Mauss I.B. To be happy and to know it: The experience and meta-awareness of pleasure.in: Kringelbach M.L. Berridge K.C. Pleasures of the Brain. Oxford University Press, Oxford, U.K.2010: 244-254Google Scholar). For example, framing effects can cause two people exposed to the same stimulus to report different subjective ratings, if one of them had a wider range of previously experienced hedonic intensities (e.g., pains of childbirth or severe injury) (Bartoshuk, 2014Bartoshuk L. The measurement of pleasure and pain.Perspect. Psychol. Sci. 2014; 9: 91-93Crossref PubMed Scopus (0) Google Scholar). In short, there is a difference between how people feel and report subjectively versus how they objectively respond with neural or behavioral affective reactions. Subjective ratings are not always more accurate about hedonic impact than objective hedonic reactions and the latter can be measured independently of the former. The experience of one pleasure often seems very different from another. Eating delicious foods, experiencing romantic or sexual pleasures, using addictive drugs, listening to music, or seeing a loved one: each feels unique. The only psychological feature in common would seem that all are pleasant. However, the difference in one’s subjective experiences is not necessarily a good guide to the underlying neural mechanisms. Those neural mechanisms may overlap to a surprising degree. Over the last decades, a growing set of results from neuroimaging studies have suggested that many diverse rewards activate a shared or overlapping brain system: a “common currency” reward network of interacting brain regions. Pleasures of food, sex, addictive drugs, friends and loved ones, music, art, and even sustained states of happiness can produce strikingly similar patterns of brain activity (Cacioppo et al., 2012Cacioppo S. Bianchi-Demicheli F. Frum C. Pfaus J.G. Lewis J.W. The common neural bases between sexual desire and love: a multilevel kernel density fMRI analysis.J. Sex. Med. 2012; 9: 1048-1054Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar, Georgiadis and Kringelbach, 2012Georgiadis J.R. 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Consistent with this, subtle differences may be found in neuronal firing in animal studies between different sensory rewards, such as tasty foods versus addictive drugs (though some neural differences may be due to accompanying confounds, such as different movements required to obtain the different reward, or sensory accompaniments, rather than to unique reward encoding per se) (Cameron and Carelli, 2012Cameron C.M. Carelli R.M. Cocaine abstinence alters nucleus accumbens firing dynamics during goal-directed behaviors for cocaine and sucrose.Eur. J. Neurosci. 2012; 35: 940-951Crossref PubMed Scopus (0) Google Scholar). Still, so far, the balance of evidence suggests rather massive overlap between neural systems that mediate rewards of different types. The overlap is far more extensive than many might have exp