‘Liking’ and ‘wanting’ in eating and food reward: Brain mechanisms and clinical implications

Highlights

• Hedonic hotspots are unique subregions within limbic structures able to causally amplify the hedonic impact of palatable tastes.

• Mesocorticolimbic incentive salience systems are more robust and able to generate ‘wanting’ independently of ‘liking’.

• Mesocorticolimbic/homeostatic mechanisms interact to generate appetite.

• Incentive-sensitization may create excessive cue-triggered ‘wanting’ to eat in some types of obesity or binge eating disorders.

Abstract

It is becoming clearer how neurobiological mechanisms generate ‘liking’ and ‘wanting’ components of food reward. Mesocorticolimbic mechanisms that enhance ‘liking’ include brain hedonic hotspots, which are specialized subregions that are uniquely able to causally amplify the hedonic impact of palatable tastes. Hedonic hotspots are found in nucleus accumbens medial shell, ventral pallidum, orbitofrontal cortex, insula cortex, and brainstem. In turn, a much larger mesocorticolimbic circuitry generates ‘wanting’ or incentive motivation to obtain and consume food rewards. Hedonic and motivational circuitry interact together and with hypothalamic homeostatic circuitry, allowing relevant physiological hunger and satiety states to modulate ‘liking’ and ‘wanting’ for food rewards. In some conditions such as drug addiction, ‘wanting’ is known to dramatically detach from ‘liking’ for the same reward, and this may also occur in over-eating disorders. Via incentive sensitization, ‘wanting’ selectively becomes higher, especially when triggered by reward cues when encountered in vulnerable states of stress, etc. Emerging evidence suggests that some cases of obesity and binge eating disorders may reflect an incentive-sensitization brain signature of cue hyper-reactivity, causing excessive ‘wanting’ to eat. Future findings on the neurobiological bases of ‘liking’ and ‘wanting’ can continue to improve understanding of both normal food reward and causes of clinical eating disorders.

Introduction

Several decades of neuroscience studies have advanced understanding of how the brain generates behavior related to food reward, motivation, and hunger. A fundamental question that remains is how mesocorticolimbic and hypothalamic circuitry interact to produce reward and the motivation to eat [1], [2], [3], [4], [5], [6], [7].

Work in our lab has focused on understanding how mesocorticolimbic systems generate ‘wanting’ and ‘liking’ for food rewards, which have turned out to be somewhat separable. Here we describe how various brain mechanisms produce those two components of food reward. ‘Wanting’ and ‘liking’ usually cohere together, but also can dissociate in particular brain conditions to come apart. Findings have revealed a distributed network of brain hedonic ‘hotspots’ that can amplify hedonic impact or ‘liking’ for food rewards. These ‘liking’ mechanisms differ from larger mesocorticolimbic circuitry that generates incentive salience or ‘wanting’ as motivation to eat. We focus on mechanisms for ‘liking’ and for ‘wanting’, and how these interact with homeostatic hypothalamic circuitry in controlling eating and food reward.

The words liking and wanting are often used interchangeably in ordinary life when talking about rewards. For example, people may want a palatable piece of chocolate because they like the flavor and other sensations of consuming it. In ordinary use, liking means conscious pleasure and wanting means conscious desire, which typically involve cognitive appraisals and declarative goals mediated by cortically-weighted circuitry. But here we use quotations for ‘wanting’ and ‘liking in order to distinguish specific psychological processes from ordinary use [8]. ‘Wanting’ here refers to the particular psychological process of incentive salience, which can occur either consciously or unconsciously, generated by brain mesolimbic circuitry in the form of cue-triggered motivation. When rewards such as palatable foods and their predictive cues are imbued with incentive salience by mesocorticolimbic circuitry, those cues and foods become attractive, and in conscious form able to elicit subjective cravings. Whether conscious or not, incentive salience triggered by cues can also generate behavioral urges to seek and consume their associated rewards [9,10]. In the laboratory, ‘wanting’ is typically measured in humans by subjective craving ratings, and in animals by how much food is pursued, consumed, or preferred over an alternative. ‘Liking’ refers to the hedonic impact of pleasant rewards, which when surfaced into consciousness can result subjective pleasure ratings in adult humans, but which in animals and infant humans can be assessed via objective measures of hedonic orofacial expressions elicited to taste in the affective taste reactivity test [11], [12], [13], [14], [15]. ‘Liking’ and ‘wanting’ can become separated in some conditions, as discussed below.

The hedonic taste reactivity task measures affective orofacial reactions to tastes of sucrose, quinine, water, etc., and the reactions to any given taste can also be shifted by a variety of relevant physiological, learning, and brain manipulation factors that alter its palatability. Originally pioneered by Steiner for use in human infants [11], the test was adapted for rodents by Grill and Norgren [13]. Orofacial responses to taste are grouped into positive, neutral, and aversive categories. Positive hedonic or ‘liking’ evaluations (Fig. 1a) are reflected in tongue protrusions, paw licks, and lateral tongue protrusions, typically elicited by tastes such as sucrose. By comparison, negative aversive or ‘disgust’ evaluations are reflected by gapes, forelimb, flails, headshakes, paw treading and face washes, and typically elicited by bitter quinine. Many of these orofacial expressions to taste are homologous, or evolutionarily conserved, across mammalian species ranging from human infants to non-human primates, rodents, and horses [14], [15], [16]. In our laboratory, rodents are implanted with bilateral oral cannula, which allow taste solutions to be directly infused into their mouths without them having to engage in any appetitive activity to obtain them, and allowing experimenter control of stimulus intensity and duration. Independence from appetitive or instrumental decisions to consume is important in allowing taste reactivity to provide a relatively pure measure of taste-elicited ‘liking’, without being altered by changes in ‘wanting’ that can influence most other behavioral measures of food reward [15,17].

Tastants with very different sensory properties like sucrose, saccharin, salt, and fats can all evoke similar positive ‘liking’ responses, indicating that hedonic reactions are palatability-specific rather than sensory-specific [14], [18], [19], [20], [21]. Accordingly, taste reactivity behaviors are not simple inflexible reflexes to a particular sensation, but rather reflect a hedonic evaluation that also depends on the internal state of the organism, including physiological appetite and satiety states, neurobiological states, as well as learned associations carried from previous experiences with the taste. Physiological states like hunger and satiety can shift subjective ratings of palatability for a particular taste in humans, in a phenomenon known as alliesthesia [22], [23], [24]. In rodents too, caloric hunger magnifies hedonic ‘liking’ reactions to palatable sweet taste, whereas satiety conversely reduces ‘liking’ [25,26]. Similarly, salt appetite modulates the hedonic impact of the intense saltiness taste of concentrated NaCl. For example, hypertonic concentrations of salt are normally aversive, in the sense that rats mostly display ‘disgust’ reactions when a seawater concentration of NaCl is placed into their mouths. However, when a hormonal state of sodium deficiency or salt depletion is induced, orofacial reactivity to the same intensely salty taste shifts to mostly positive ‘liking’ [20,[27], [28], [29], [30], [31]]. Conversely, modulation by learned associations can be induced by pairing a novel ‘liked’ sweet taste of saccharin as a Pavlovian conditioned stimulus (CS+) with an injection of lithium chloride, which induces malaise, as an unconditioned stimulus (UCS), to produce a conditioned taste aversion (CTA) so that subsequent exposures to saccharin taste instead elicit negative gapes and related ‘disgust’ reactions [32], [33], [34], [35], [36], [37].

Our laboratory has studied brain generators of taste ‘liking’ by combining central neural manipulations of hedonic circuitry with the taste reactivity measure of ‘liking’ versus ‘disgust’. In brief, pharmacological microinjections, excitotoxin lesions, optogenetic brain stimulation or inhibitions, etc. are used to systematically turn on or turn off particular neural systems in various brain locations during the taste reactivity test. This is coupled with an analysis of local Fos protein expression that allows us to more directly determine the spread of neuronal changes induced by a manipulation that alters ‘liking’, to identify localization of function, and map subregional localization of hedonic mechanisms within a brain structure. These studies have revealed a distributed network of limbic hotspots or small sites within subregions of cortical and subcortical structures in the rat that are capable of amplifying the hedonic impact (Fig. 1b) of sucrose taste [19,[38], [39], [40]]. Brain hedonic hotspots appear to be restricted to particular subregions of limbic structures such as rostrodorsal quadrant of medial shell of nucleus accumbens (NAc), caudolateral half of ventral pallidum (VP), a rostromedial portion orbitofrontal cortex (OFC), a far posterior zone of insula cortex (IC), and the parabrachial nucleus of the brainstem pons (PBN). Brain hedonic hotspots that generate ‘liking’ are embedded within larger mesocorticolimbic circuitry (spanning several entire structures) that is capable of generating incentive salience ‘wanting’, underlying the close interconnection between ‘liking’ and ‘wanting’ functions in reward [38,[41], [42], [43], [44], [45], [46], [47], [48]]. In the following sections we discuss roles of these hedonic hotspots and mesocorticolimbic motivation circuitry in food reward, describe recent findings, and consider their potential roles in normal appetite and in clinical eating disorders and obesity.