Reward signalling in brainstem nuclei under fluctuating blood glucose

Phasic dopamine release from mid-brain dopaminergic neurons is thought to signal errors of reward prediction (RPE). If reward maximisation is to maintain homeostasis, then the value of primary rewards should be coupled to the homeostatic errors they remediate. This leads to the prediction that RPE signals should be configured as a function of homeostatic state and thus diminish with the attenuation of homeostatic error. To test this hypothesis, we collected a large volume of functional MRI data from five human volunteers on four separate days. After fasting for 12 hours, subjects consumed preloads that differed in glucose concentration. Participants then underwent a Pavlovian cue-conditioning paradigm in which the colour of a fixation-cross was stochastically associated with the delivery of water or glucose via a gustometer. This design afforded computation of RPE separately for better- and worse-than expected outcomes during ascending and descending trajectories of serum glucose fluctuations. In the parabrachial nuclei, regional activity coding positive RPEs scaled positively with serum glucose for both ascending and descending glucose levels. The ventral tegmental area and substantia nigra became more sensitive to negative RPEs when glucose levels were ascending. Together, the results suggest that RPE signals in key brainstem structures are modulated by homeostatic trajectories of naturally occurring glycaemic flux, revealing a tight interplay between homeostatic state and the neural encoding of primary reward in the human brain.

Secondary rewards acquire enhanced incentive motivation via increasing anticipatory activity of the lateral orbitofrontal cortex

The motivation to strive for and consume primary rewards such as palatable food is bound by internal satiation and devaluation mechanisms, yet secondary rewards such as money may not be bound by these regulatory mechanisms. The present study therefore aimed at determining diverging devaluation trajectories for primary (chocolate milk) and secondary (money) reinforcers on the behavioral and neural level. Satiation procedures combined with a choice (Experiment 1) and an incentive delay (Experiment 2) paradigm consistently revealed decreased hedonic value for the primary reward as reflected by decreasing hedonic evaluation and choice preference, while hedonic value and preferences for the secondary reward increased. Concomitantly acquired functional near-infrared spectroscopy (fNIRS) data during the incentive delay paradigm revealed that increasing value of the secondary reward was accompanied by increasing anticipatory activation in the lateral orbitofrontal cortex, while during the consummatory phase the secondary reinforcer associated with higher medial orbitofrontal activity irrespective of devaluation stage. Overall, the findings suggest that – in contrast to primary reinforcers - secondary reinforcers can acquire progressively enhanced incentive motivation with repeated receipt, suggesting a mechanism which could promote escalating striving to obtain secondary rewards.

A selective effect of dopamine on information-seeking

Humans are motivated to seek information from their environment. How the brain motivates this behavior is unknown. One speculation is that the brain employs neuromodulatory systems implicated in primary reward-seeking, in particular dopamine, to instruct information-seeking. However, there has been no causal test for the role of dopamine in information-seeking. Here, we show that administration of a drug that enhances dopamine function (dihydroxy-L-phenylalanine; L-DOPA) reduces the impact of valence on information-seeking. Specifically, while participants under Placebo sought more information about potential gains than losses, under L-DOPA this difference was not observed. The results provide new insight into the neurobiology of information-seeking and generates the prediction that abnormal dopaminergic function (such as in Parkinson’s disease) will result in valence-dependent changes to information-seeking.

Neural Circuitry of Information Seeking

Humans and animals navigate uncertain environments by seeking information about the future. Remarkably, we often seek information even when it has no instrumental value for aiding our decisions – as if the information is a source of value in its own right. In recent years, there has been a flourishing of research into these non-instrumental information preferences and their implementation in the brain. Individuals value information about uncertain future rewards, and do so for multiple reasons, including valuing resolution of uncertainty and overweighting desirable information. The brain motivates this information seeking by tapping into some of the same circuitry as primary rewards like food and water. However, it also employs cortex and basal ganglia circuitry that predicts and values information as distinct from primary reward. Uncovering how these circuits cooperate will be fundamental to understanding information seeking and motivated behavior as a whole, in our increasingly complex and information-rich world.

Reward signalling in brainstem nuclei under glycemic flux

Phasic dopamine release from mid-brain dopaminergic neurons signals errors of reward prediction (RPE). If reward maximisation is to maintain homeostasis, then the value of primary rewards should be coupled to the homeostatic errors they remediate. This leads to the prediction that RPE signals should be configured as a function of homeostatic state and thus, diminish with the attenuation of homeostatic error. To test this hypothesis, we collected a large volume of functional MRI data from five human volunteers on four separate days. After fasting for 12 hours, subjects consumed preloads that differed in glucose concentration. Participants then underwent a Pavlovian cue-conditioning paradigm in which the colour of a fixation-cross was stochastically associated with the delivery of water or glucose via a gustometer. This design afforded computation of RPE separately for better- and worse-than expected outcomes during ascending and descending trajectories of physiological serum glucose fluctuations. In the parabrachial nuclei, variations in regional activity coding positive RPEs scaled positively with serum glucose for ascending and descending glucose levels. The ventral tegmental area and substantia nigra became more sensitive to negative RPEs when glucose levels were ascending. Together, the results show that RPE signals in key brainstem structures are modulated by homeostatic trajectories of naturally occurring glycemic flux, revealing a tight interplay between homeostatic state and the neural encoding of primary reward in the human brain.

Caloric Primary Rewards Systematically Alter Time Perception

Human time perception can be influenced by contextual factors, such as the presence of reward. Yet, the exact nature of the relationship between time perception and reward has not been conclusively characterized. We implemented a novel experimental paradigm to measure estimations of time across a range of suprasecond intervals, during the anticipation and after the consumption of fruit juice, a physiologically relevant primary reward. We show that average time estimations were systematically affected by the consumption of reward, but not by the anticipation of reward. Compared with baseline estimations of time, reward consumption was associated with subsequent overproductions of time, and this effect increased for larger magnitudes of reward. Additional experiments demonstrated that the effect of consumption did not extend to a secondary reward (money), a tasteless, noncaloric primary reward (water), or a sweet, noncaloric reward (aspartame). However, a tasteless caloric reward (maltodexrin) did induce overproductions of time, although this effect did not scale with reward magnitude. These results suggest that the consumption of caloric primary rewards can alter time perception, which may be a psychophysiological mechanism by which organisms regulate homeostatic balance.

Other Floral Rewards

This chapter examines a variety of rewards that can be obtained by pollinators from flower visits, including oils, waxes, scents, and resins and gums. Fatty oils as an offering in flowers are now known from at least eighty genera across several families and from nearly 1 per cent of flowering plant species. Floral resins have been reported in occasional genera that are abundant in the tropics. The chapter also considers stigmatic exudates, which provide a good oily food source that sometimes can be the primary reward; examples of fragrance as a reward; floral tissues; and other possible nonfood rewards such as brood sites, microclimatic protection and warmth, and meeting places. Most of the rewards discussed in this chapter may be the key to some particularly fascinating pollination systems and open up possibilities for new dimensions in animal–flower interactions.

Rewards 1: The Biology of Pollen

This chapter examines the biology of pollen, the primary reward for flowers in an evolutionary sense and probably the resource for which animals first went to flowers. The inherent characteristics of pollen make it a useful resource to exploit as food, potentially collectable by almost any animal. It remains a crucial reward for pollen-eating and pollen-gathering visitors, such as some flies, some beetles, and virtually all bees. Pollen’s function as a reward of visitors is mutually incompatible with its function in reproduction. The chapter first describes the characteristics of pollen grains before discussing the storage and delivery of pollen in the plant. It then considers pollen packaging, pollen gathering by animals, pollen as food, and pollen preferences. It also explores the longevity and viability of pollen, pollen-only flowers, and pollen competition. Finally, it reflects on the question of how much pollen a plant “should” produce.