Elsevier

Neuroscience

Volume 126, Issue 4, 2004, Pages 807-819
Neuroscience

Review
Food for thought: hedonic experience beyond homeostasis in the human brain

https://doi.org/10.1016/j.neuroscience.2004.04.035Get rights and content

Abstract

Food intake is an essential human activity regulated by homeostatic and hedonic systems in the brain which has mostly been ignored by the cognitive neurosciences. Yet, the study of food intake integrates fundamental cognitive and emotional processes in the human brain, and can in particular provide evidence on the neural correlates of the hedonic experience central to guiding behaviour. Neuroimaging experiments provide a novel basis for the further exploration of the brain systems involved in the conscious experience of pleasure and reward, and thus provide a unique method for studying the hedonic quality of human experience. Recent neuroimaging experiments have identified some of the regions involved in the cortical networks mediating hedonic experience in the human brain, with the evidence suggesting that the orbitofrontal cortex is the perhaps strongest candidate for linking food and other kinds of reward to hedonic experience. Based on the reviewed literature, a model is proposed to account for the roles of the different parts of the orbitofrontal cortex in this hedonic network.

Section snippets

Food intake

Food intake is a precisely controlled act that can potentially be fatal if the wrong decision is taken to swallow toxins, microorganisms or non-food objects on the basis of erroneously determining the sensory properties of the food. Humans have therefore developed elaborate food behaviours which are aimed at balancing conservative risk-minimising and life-preserving strategies with occasional novelty seeking in the hope of discovering new sources of nutrients (Rozin, 2001).

Food intake must

Motivation and emotion

Food motivation (and motivation in general) is closely related to emotion and is generally defined in opposition to cognition as that which moves us in some way, as implied by the common Latin root of both words (movere, to move). It is only recently that the fields of motivation and emotion have tended to go different ways, and have in the past been considered together (Gray, 1975, Papez, 1937, Rolls, 1999, Weiskrantz, 1968). One often used functional distinction between motivation and emotion

Human sensory systems and food intake

Most of our sensory systems are involved in the regulation of food intake. Whilst Aristotle and other ancient philosophers proposed only five senses (sight, hearing, smell, taste, and touch), it is clear that many other senses exist such as e.g. the sensory receptors in the digestive tract which are sensitive to e.g. gastric distension, and those in the circulatory system that are sensitive to changes in blood pressure or carbon dioxide gas in the blood.

Potential food sources can be evaluated

Taste

Taste is sensed by taste receptor cells arranged in taste buds which are primarily found on the tongue but also on other areas in the oral cavity such as the soft palate, the pharynx, the larynx and the epiglottis (Scott and Plata-Salaman, 1999). Taste receptor cells are constantly being renewed and have a turnover period of between 7 and 10 days. As a convenient way of organising the taste system, most researchers agree that there are four different taste qualities with specific receptor

Smell

Smell is sensed by olfactory receptors placed in the upper part of the nasal cavity. There are about 100 million bipolar olfactory cells in humans with lifelong continuous replacement every 4–8 weeks from stem cells in the sensory epithelium. Each bipolar olfactory cell bears up to a thousand hairs (cilia), which are the points of contact for aromatic molecules. The cilia must be moistened continuously by mucous glands roughly every 10 min to avoid desiccation. The mucus consists of a water

Multimodal integration

In addition to multimodal information from taste and smell, decisions about food intake also integrate e.g. somatosensory information, which is sensed by receptors in the oral and nasal cavity. This sensory information includes temperature, viscosity, fat contents, pungency and irritation and is mediated by a large variety of neural systems. This integrated information is processed and made available for the crucial decision of ingestion or rejection of a potentially poisonous food (although,

Reward in the human brain

Multiple reward systems have been demonstrated in the mammalian brain (Rolls, 1999, Panksepp, 1998, Robbins et al., 1989, Wise, 1996). Many successful animal models have explored reward-learning mechanisms related to various forms of classical and instrumental conditioning. Until recently, however, not much was known about hedonic processes in the human brain. These hedonic systems are now being explored using novel neuroimaging experiments that provide evidence of activity in brain regions

Hedonics

Historically, the research on reward and motivation was initially focussed on intra-cranial self-stimulation (Liebman, 1983, Milner, 1991, Olds and Olds, 1963) and drug addiction (Wise, 1996, Berke and Hyman, 2000), which has led to the identification of brain reward systems that allow reinforcement of responses without homeostatic value. Some studies have, however, suggested that food and drug rewards may share common neural circuits and neurotransmitters which include opioid receptors (

Taste

The results of investigating the hedonic processes associated with pure taste in the human brain confirm that dissociable brain areas are involved in the representation of the identity and the hedonics of the stimulus. The primary gustatory areas have been investigated using neuroimaging with pure sweet, salt, sour, bitter and umami stimuli, and consistent with neurophysiological studies in non-human primates found to be located in the anterior insula/frontal operculum and caudal orbitofrontal

Olfaction

Similar to taste stimuli, pure olfactory stimuli activate dissociable brain areas for motivation-independent representations of reinforcer identity and hedonic representations. Neuroimaging studies have found representations of olfactory identity in primary olfactory cortices (Anderson et al., 2003, Gottfried et al., 2002a, O'Doherty et al., 2000, Rolls et al., 2003a, Royet et al., 2000, Royet et al., 2001, Zald and Pardo, 1997), which are distinct from hedonic representations in other brain

Multimodal stimuli

The evidence from neuroimaging studies of pure taste and smell thus shows that the orbitofrontal cortex is consistently correlated with the subjective pleasantness ratings of the stimuli. Therefore, it is to be expected that studies using multi-modal combinations of taste and smell should find correlations between pleasantness and activity in these brain regions. Compelling evidence that this is indeed the case comes from a sensory-specific satiety neuroimaging study which has shown that a

Other sensory modalities

Further neuroimaging studies have investigated the hedonic systems involved in other sensory modalities and, consistent with the results obtained with food relevant stimuli, activations were found that link hedonic processing to activity in the orbitofrontal cortex.

In a study of thermal stimulation it was found that the perceived thermal intensity was correlated with activity in the insula and orbitofrontal cortices (Craig, 2002, Craig et al., 2000). In another study investigating the effects

Lesion studies

Neuroimaging studies are essentially only correlative measures of behaviour, and it is therefore important to briefly consider the evidence from lesions in both humans and higher primates to assess the validity of the findings. In humans, damage to the orbitofrontal cortex causes major changes in motivation, emotion, personality, behaviour, and social conduct. A classic case of orbitofrontal damage is that of Phineas Gage, whose medial frontal lobes were penetrated by a metal rod (Harlow, 1848

Conclusions

Food intake is essential to sustain life, and the sensory systems of taste and smell are amongst the most fundamental building blocks of the brain's natural reward systems (Kelley and Berridge, 2002). Humans' large so-called higher cognitive functions have evolved to support the required cognitive processing involved in the sophisticated foraging needed for the sustained food intake needed for omnivores such as humans. However, with the current state of overabundance of food in the developed

Acknowledgements

This research is supported by the Wellcome Trust and the MRC (to FMRIB). The author would like to thank Caroline Andrews, Annie Cattrell, Phil Cowen, Ivan De Araujo, Peter Hobden, Julia Hornak, John O'Doherty, Edmund Rolls, Birgit Völlm and James Wilson for their collaboration on some of the work reviewed here. Furthermore, the helpful points raised by the two anonymous reviewers are gratefully acknowledged.

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