Affective neuroscience of pleasure: reward in humans and animals

Abstract

Introduction: Pleasure and reward are generated by brain circuits that are largely shared between humans and other animals.

Discussion: Here, we survey some fundamental topics regarding pleasure mechanisms and explicitly compare humans and animals.

Conclusion: Topics surveyed include liking, wanting, and learning components of reward; brain coding versus brain causing of reward; subjective pleasure versus objective hedonic reactions; roles of orbitofrontal cortex and related cortex regions; subcortical hedonic hotspots for pleasure generation; reappraisals of dopamine and pleasure-electrode controversies; and the relation of pleasure to happiness.

Fig. 1

Hedonic hotspots and hedonic circuits. Hedonic hotspots are shown in nucleus accumbens, ventral pallidum, and brainstem parabrachial nucleus where opioid or other signals cause amplification of core ‘liking’ reactions to sweetness. Reprinted with permission from Smith et al. (2008), based on Kringelbach (2005), Peciña et al. (2006), and Smith and Berridge (2007)

Fig. 2

Taste ‘liking’ reactions and contrast map of nucleus accumbens hotspots. Positive ‘liking’ reactions to pleasant sweet tastes shared by human newborn, young orangutan, and adult rat (tongue protrusion, left top) and aversive ‘disliking’ reactions to unpleasant bitter tastes (gape, left bottom). Opioid hotspots and coldspots in the nucleus accumbens (medial shell region shown in sagittal view, right). Green The entire medial shell mediates opioid-stimulated increases in ‘wanting’ for food reward. Red Only a cubic-millimeter-sized hedonic hotspot generates increases in ‘liking’ for the same opioid stimulation. Blue A small hedonic ‘coldspot’ suppresses ‘liking’ reactions to sucrose, whereas a larger purple zone suppresses ‘disliking’ reactions to quinine. Reprinted with permission from Smith et al. (2008), based on data from Peciña and Berridge (2005)

Fig. 3

Valence coding in medial OFC. a The activity in medial OFC correlates with the subjective ratings of pleasantness in an experiment with three pleasant and three unpleasant odors (Rolls et al. 2003). b Similarly, the activity in medial OFC was also correlated with the subjective pleasantness ratings of water in a thirst experiment (de Araujo et al. 2003b). A correlation in a very similar part of medial OFC was found with the pleasantness of other pure tastants used in the experiment (not shown). c This corresponded to the findings in an experiment investigating taste and smell convergence and consonance, which found that activity in the medial OFC was correlated with subjective consonance ratings (de Araujo et al. 2003c). d Even higher-order rewards such as monetary reward were found to correlate with activity in the medial OFC (O’Doherty et al. 2001)

Fig. 4

Hedonic experience. a The activity in mid-anterior parts of the orbitofrontal cortex correlated with the subjective pleasantness ratings of the foods (Kringelbach et al. 2003). On the right is shown the magnitude of the fitted hemodynamic response from a representative subject plotted against the subjective pleasantness ratings (on a scale from −2 to +2) and peristimulus time in seconds. b Additional evidence for the role of the mid-anterior orbitofrontal cortex in subjective experience comes from another neuroimaging experiment investigating the supra-additive effects of combining the umami tastants monosodium glutamate and inosine monophosphate (de Araujo et al. 2003a). The figure shows the region of mid-anterior orbitofrontal cortex showing synergistic effects (rendered on the ventral surface of human cortical areas with the cerebellum removed). The synergy is unlikely to be expressed in the taste receptors themselves, and the activity in the orbitofrontal cortex may thus reflect the subjective enhancement of umami taste, which must be closely linked to subjective experience. c Adding strawberry odor to a sucrose taste solution makes the combination more pleasant than the sum of each of the individual components. The supra-linear effects on subjective enhancement activated a lateral region of the left mid-anterior orbitofrontal cortex, similar to as found in other experiments (de Araujo et al. 2003c). d These findings were strengthened by findings using DBS and MEG (Kringelbach et al. 2007a). Pleasurable subjective pain relief for chronic pain in a phantom limb in a patient was causally induced by effective deep brain stimulation in the PVG/PAG part of the brainstem. When using MEG to directly measure the concomitant changes in the rest of the brain, a significant change in power was found in the mid-anterior OFC

Fig. 5

Model of the functions of the orbitofrontal cortex. a The proposed model shows the interactions between sensory and hedonic systems in the orbitofrontal cortex using as an example one hemisphere of the orbitofrontal cortex (Kringelbach 2004). Information is flowing from bottom to top on the figure. Sensory information arrives from the periphery to the primary sensory cortices, where the stimulus identity is decoded into stable cortical representations. This information is then conveyed for further multimodal integration in brain structures in the posterior parts of the orbitofrontal cortex. The reward value of the reinforcer is assigned in more anterior parts of the orbitofrontal cortex from where it can then be used to influence subsequent behavior (in lateral parts of the anterior orbitofrontal cortex with connections to anterior cingulate cortex), stored for valence learning/memory (in medial parts of the anterior orbitofrontal cortex), and made available for subjective hedonic experience (in mid-anterior orbitofrontal cortex). The reward value and the subjective hedonic experience can be modulated by hunger and other internal states. b In addition, there is important reciprocal information flowing between the various regions of the orbitofrontal cortex and other brain regions as demonstrated by the detailed inputs between the different sub-regions

Fig. 6

Orbitofrontal cortex (OFC) comparison in rats and primates. Homology between the prefrontal cortex in rat (orbital and agranular insular areas) and primates (OFC) is indicated by their similar patterns of connectivity with the mediodorsal thalamus (MD, green), amygdala (orange), and striatum/accumbens/pallidum system (pink). In both species, the OFC receives robust sensation input from sensory cortices and associative information from the amygdala, and in both sends motor and limbic outputs to the striatum and nucleus accumbens. A coronal example is shown in each box. AId Dorsal agranular insula, AIv ventral agranular insula, c central, CD caudate, LO lateral orbital, m medial, NAc nucleus accumbens core, rABL rostral basolateral amygdala, VO ventral orbital, including ventrolateral and ventromedial orbital regions, VP ventral pallidum. Reprinted with permission from Schoenbaum et al. (2006)

Fig. 7

Pleasure electrodes or not? Comparison of famous examples of controversial ‘pleasure electrodes’ in rat (from Olds 1961) and in human (patient B-19, a young man, from Heath 1972). Thick black lines show the electrodes (insulated except at tip; red dots indicate their stimulating tips). Both the rat and the human pressed for electrode stimulation up to thousands of times, but recently questions have been raised whether both electrodes might have produced merely a pure form of ‘wanting’ (incentive salience) rather than actual ‘liking’ (true hedonic pleasure). Reprinted from Smith et al. (2008)