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The Human Orbitofrontal Cortex: Linking Reward to Hedonic Experience

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The Human Orbitofrontal Cortex: Linking Reward to Hedonic Experience REVIEWS THE HUMAN ORBITOFRONTAL CORTEX: LINKING REWARD TO HEDONIC EXPERIENCE Morten L. Kringelbach Abstract | Hedonic experience is arguably at the heart of what makes us human. In recent neuroimaging studies of the cortical networks that mediate hedonic experience in the human brain, the orbitofrontal cortex has emerged as the strongest candidate for linking food and other types of reward to hedonic experience. The orbitofrontal cortex is among the least understood regions of the human brain, but has been proposed to be involved in sensory integration, in representing the affective value of reinforcers, and in decision making and expectation. Here, the functional neuroanatomy of the human orbitofrontal cortex is described and a new integrated model of its functions proposed, including a possible role in the mediation of hedonic experience. REINFORCERS The human orbitofrontal cortex has received relatively expansion and heterogeneous nature of this brain Positive reinforcers (rewards) little attention in studies of the prefrontal cortex, and region mean that a full understanding of its functions increase the frequency of many of its functions remain enigmatic. During pri- must be informed by evidence from human neuro- behaviour that leads to their mate evolution, the orbitofrontal cortex has developed imaging and neuropsychology studies. acquisition. Negative reinforcers (punishers) decrease the considerably, and although some progress has been Recently, neuroimaging studies have found that 3 4 frequency of behaviour that made through neurophysiological recordings in non- the reward value , the expected reward value and leads to their encounter and human primates, it is only during the past couple of even the subjective pleasantness of foods5 and other increase the frequency of years that evidence has converged from neuroimag- REINFORCERS are represented in the orbitofrontal cortex. behaviour that leads to their ing, neuropsychology and neurophysiology to allow Such findings could provide a basis for further explo- avoidance. a better understanding of the functions of the human ration of the brain systems involved in the conscious orbitofrontal cortex. These studies indicate that the experience of pleasure and reward, and, as such, orbitofrontal cortex is a nexus for sensory integration, provide a unique method for studying the hedonic University of Oxford, the modulation of autonomic reactions, and partici- quality of human experience. In particular, the links University Laboratory of pation in learning, prediction and decision making of the orbitofrontal cortex and related areas with Physiology, Parks Road, for emotional and reward-related behaviours. The the sensory and rewarding properties of reinforcers Oxford OX1 3PT, UK, and orbitofrontal cortex functions as part of various net- might offer important insights into emotional disor- FMRIB, Oxford Centre for works that include regions of the medial prefrontal ders such as depression, and the current worldwide Functional Magnetic Resonance Imaging of the cortex, hypothalamus, amygdala, insula/operculum obesity epidemic. Brain, John Radcliffe and dopaminergic midbrain, and areas in the basal Hospital, Headley Way, ganglia including the ventral and dorsal striatum. Neuroanatomy of the orbitofrontal cortex Oxford OX3 9DU, UK. These additional areas have been investigated in detail The orbitofrontal cortex occupies the ventral surface e-mail: morten.kringelbach@ in rodents and other animals, and have been described of the frontal part of the brain (FIGS 1,2). It is defined as 1,2 physiol.ox.ac.uk in other reviews . Here, I focus on the functions of the part of the prefrontal cortex that receives projec- doi:10.1038/nrn1748 the human orbitofrontal cortex, as the phylogenetic tions from the magnocellular medial nucleus of the NATURE REVIEWS | NEUROSCIENCE VOLUME 6 | SEPTEMBER 2005 | 691 REVIEWS a 4 6 3 1 1 2 6 4 3 2 8 5 5 7 8 7 9 9 32 31 24 23 19 19 33 10 40 18 10 26 39 29 18 30 45 27 44 43 41 34 35 42 17 47 22 11 25 28 36 18 11 38 19 21 17 38 37 18 37 19 20 20 bc d 9 24c 6 8B 9 24b SC 6 CC 24a 25 8B 32 10m 10 9 24 24 TT 25 SR CC 10 14l OB 32 14c 14 25 PrCO G Iapl 12l 12o Ial 47/12 Iai 13l Iapm 12 12r 12m FM 11l 13mIam PC 13 13b 13a AON 11 OS 13 11 10o11m OT OT 10 14r 14c 10 14 25 OB LOT Figure 1 | Cytoarchitectonic maps of human and monkey orbitofrontal cortices. a | Brodmann’s original cytoarchitectonic maps of the human brain with a ventral view of the brain on the left and a medial view of the cortical areas on the medial wall of the brain on the right8,111. The complex cytoarchitecture of the orbitofrontal cortex was reduced to three areas, 11, 47 and 10. b | Later investigations further subdivided the orbitofrontal cortex to reflect its heterogeneity, as first proposed in the maps of Walker. Views of the medial wall and ventral surface are shown for the monkey Macaca fascicularis. Walker proposed a further parcellation of the orbitofrontal cortex into five areas (areas 10, 11, 12, 13 and 14). FM, sulcus frontomarginalis; OS, sulcus orbitalis; SC, sulcus callosomarginalis; SR, sulcus rostralis. c | Walker’s nomenclature was then reconciled with that used in Brodmann’s primate and human brains by Petrides and Pandya10, with lateral parts of the orbitofrontal cortex designated area 47/12. CC, corpus callosum; OT, olfactory tubercle. d | Even further subdivisions of the orbitofrontal cortex were subsequently proposed by Carmichael and Price11. AON, anterior olfactory nucleus; G, gustatory cortex; Iai, intermediate agranular insula area; Ial, lateral agranular insula area; Iam, medial agranular insula area; Iapl, posterolateral agranular insula area; Iapm, posteromedial agranular insula area; LOT, lateral olfactory tract; OB, olfactory bulb; PC, piriform cortex; PrCO, precentral opercular cortex; TT, tenia tectum. Panel a modified from REF. 8. Panel b modified from REF. 9. Panel c modified, with permission, from REF. 10 © (1994) Elsevier Science. Panel d modified, with permission, from REF. 11 © (2000) John Wiley & Sons. mediodorsal thalamus6. This is in contrast to areas of the primate (Cercopithecus) brain, in which different the prefrontal cortex that receive projections from other cytoarchitectonic areas were assigned unique numbers parts of the mediodorsal thalamus. For example, the (FIG. 1a). Unfortunately, he did not investigate the orbito- dorsolateral prefrontal cortex (BRODMANN’S AREA (BA) frontal cortex in detail, and his maps of the human BRODMANN’S AREAS 46/9) receives projections from the parvocellular lat- brain include only three orbito frontal cortical areas (BA). Korbinian Brodmann eral part of the mediodorsal thalamic nucleus, whereas — 10, 11 and 47. Furthermore, his nomenclature was (1868–1918) was an anatomist who divided the cerebral cortex the frontal eye fields in the anterior bank of the arcuate not consistent across species: area 11 in the primate map into numbered subdivisions on sulcus (BA 8) receive projections from the paralamel- is extended laterally, and area 12 takes over the medial the basis of cell arrangements, lar part of the mediodorsal thalamic nucleus. This is a area that is occupied by area 11 in the human map, types and staining properties broad connectional topography, in which each specific whereas area 47 is not included at all in the non-human (for example, the dorsolateral prefrontal cortex contains portion of the mediodorsal thalamus is connected to primate map. several subdivisions, including more than one architectonic region of the prefrontal Some clarification of the cross-species inconsisten- BA 46 and BA 9). Modern cortex7, and a better definition therefore includes cies that are present in Brodmann’s maps was provided derivatives of Brodmann’s maps each cortical area’s cortico-cortical connectivity and by Walker9, who investigated the monkey species are commonly used as the morphological features. Macaca fascicularis. He found the orbitofrontal cortex reference system for the 8 discussion of brain-imaging Brodmann carried out one of the first compre- to be much less homogeneous than Brodmann had findings. hensive cytoarchitectural analyses of the human and specified, and he proposed parcellating the primate 692 | SEPTEMBER 2005 | VOLUME 6 www.nature.com/reviews/neuro REVIEWS a Right x Left However, this left the problem of area 47 from the +60 +50 +40 +30 +20 +10 0 –10 –20 –30 –40 –50 –60 human map, which was still not included in Walker’s 70 70 map. Petrides and Pandya10 subsequently tried to 10o reconcile the remaining inconsistencies between the 60 60 human and monkey cytoarchitectonic maps by label- 50 47/12r 50 ling the lateral parts of the orbitofrontal gyri as 47/12 11m 45 11l (FIG. 1c). Further subdivisions of the orbito frontal 40 40 cortex were later proposed on the basis of nine y different histochemical and immunohistochemical 30 13m 47/12l 45 30 11 (FIG. 1d) 14r stains . 13l 20 13b 20 47/12m Two important cytoarchitectonic features of the 47/12s orbitofrontal cortices are the phylogenetic differ- 10 14c lal 10 13a lam AON lai ences BOX 1 and the considerable variability between lapm 12,13 0 0 individuals (FIG. 2). The former poses potential problems when trying to understand functional relation ships across species, and the latter poses inter- b Type 1 Type 2 Type 3 esting methodo logical challenges for those who hope to normalize individual brains to a template brain to allow them to explore the functional anatomy of the human orbitofrontal cortex. The orbitofrontal cortex receives inputs from the five classic sensory modalities: gustatory, olfactory, somatosensory, auditory and visual14. It also receives visceral sensory information, and all this input makes the orbitofrontal cortex perhaps the most polymodal region in the entire cortical mantle, with the possi- c ble exception of the rhinal regions of the temporal lobes15. The orbitofrontal cortex also has direct reciprocal connections with other brain structures, including the amygdala16,17, cingulate cortex18,19, insula/operculum20, hypothalamus21, hippocampus22, striatum23, periaque- ductal grey21 and dorsolateral prefrontal cortex14,24.
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