The functions of the orbitofrontal cortex
Introduction
The prefrontal cortex is the cortex that receives projections from the mediodorsal nucleus of the thalamus (with which it is reciprocally connected) and is situated in front of the motor and premotor cortices (areas 4 and 6) in the frontal lobe. Based on the divisions of the mediodorsal nucleus, the prefrontal cortex may be divided into three main regions (Fuster, 1997). First, the magnocellular, medial, part of the mediodorsal nucleus projects to the orbital (ventral) surface of the prefrontal cortex (which includes areas 13 and 12). It is called the orbitofrontal cortex, and receives information from the ventral or object processing visual stream, and taste, olfactory, and somatosensory inputs. Second, the parvocellular, lateral, part of the mediodorsal nucleus projects to the dorsolateral prefrontal cortex. This part of the prefrontal cortex receives inputs from the parietal cortex, and is involved in tasks such as spatial short-term memory tasks (Fuster, 1997; see Rolls & Treves, 1998). Third, the pars paralamellaris (most lateral) part of the mediodorsal nucleus projects to the frontal eye fields (area 8) in the anterior bank of the arcuate sulcus.
The functions of the orbitofrontal cortex are considered here. This analysis provides a basis for investigations of how its functions develop in ontogeny. The cortex on the orbital surface of the frontal lobe includes area 13 caudally, and area 14 medially, and the cortex on the inferior convexity includes area 12 caudally and area 11 anteriorly (see Fig. 1 and Carmichael & Price, 1994; Öngür & Price 2000; Petrides & Pandya, 1994; note that the names and numbers that refer to particular subregions are not uniform across species and investigators). This brain region is relatively poorly developed in rodents, but well developed in primates including humans. To understand the function of this brain region in humans, the majority of the studies described were therefore performed with macaques or with humans.
Section snippets
Connections
Rolls, Yaxley, and Sienkiewicz (1990) discovered a taste area in the lateral part of the orbitofrontal cortex, and showed that this was the secondary taste cortex in that it receives a major projection from the primary taste cortex (Baylis, Rolls, & Baylis, 1994). More medially, there is an olfactory area (Rolls & Baylis, 1994). Anatomically, there are direct connections from the primary olfactory cortex, pyriform cortex, to area 13a of the posterior orbitofrontal cortex, which in turn has
Effects of lesions of the orbitofrontal cortex
Macaques with lesions of the orbitofrontal cortex are impaired at tasks which involve learning about which stimuli are rewarding and which are not, and especially in altering behaviour when reinforcement contingencies change. The monkeys may respond when responses are inappropriate, e.g., no longer rewarded, or may respond to a non-rewarded stimulus. For example, monkeys with orbitofrontal damage are impaired on Go/NoGo task performance, in that they go on the NoGo trials (Iversen & Mishkin,
Taste
One of the recent discoveries that has helped us to understand the functions of the orbitofrontal cortex in behaviour is that it contains a major cortical representation of taste (see Rolls, 1989, Rolls, 1995a, Rolls, 1997a; Rolls & Scott, 2003; cf Fig. 2). Given that taste can act as a primary reinforcer, that is without learning as a reward or punishment, we now have the start for a fundamental understanding of the function of the orbitofrontal cortex in stimulus–reinforcement association
A neurophysiological basis for stimulus–reinforcement learning and reversal in the orbitofrontal cortex
The neurophysiological, imaging, and lesion evidence described suggests that one function implemented by the orbitofrontal cortex is rapid stimulus–reinforcement association learning, and the correction of these associations when reinforcement contingencies in the environment change. To implement this, the orbitofrontal cortex has the necessary representation of primary reinforcers, including taste and somatosensory stimuli. It also receives information about objects, e.g., visual
Neuropsychology
It is of interest that a number of the symptoms of frontal lobe damage in humans appear to be related to this type of function, of altering behaviour when stimulus–reinforcement associations alter, as described next. Thus, humans with frontal lobe damage can show impairments in a number of tasks in which an alteration of behavioural strategy is required in response to a change in environmental reinforcement contingencies (see Goodglass & Kaplan, 1979; Jouandet & Gazzaniga, 1979; Kolb & Whishaw,
Stimulus–reinforcement association and reversal
This reversal learning that occurs in the orbitofrontal cortex could be implemented by Hebbian modification of synapses conveying visual input onto taste-responsive neurons, implementing a pattern association network (Rolls, 1999, Rolls, 2000f; Rolls & Treves, 1998; Rolls & Deco, 2002). Long-term potentiation would strengthen synapses from active conditional stimulus neurons onto neurons responding to a primary reinforcer such as a sweet taste, and homosynaptic long-term depression would weaken
Conclusions and summary
The orbitofrontal cortex contains the secondary taste cortex, in which the reward value of taste is represented. It also contains the secondary and tertiary olfactory cortical areas, in which information about the identity and also about the reward value of odours is represented. The orbitofrontal cortex also receives information about the sight of objects from the temporal lobe cortical visual areas, and neurons in it learn and reverse the visual stimulus to which they respond when the
Acknowledgments
The author have worked on some of the experiments described here with I. Araujo, L.L. Baylis, G.C. Baylis, R. Bowtell, A.D. Browning, H.D. Critchley, S. Francis, M.E. Hasselmo, J. Hornak, M. Kadohisa, M. Kringelbach, C.M. Leonard, F. McGlone, F. Mora, J. O'Doherty, D.I. Perrett, T.R. Scott, S.J. Thorpe, J. Verhagen, E.A. Wakeman, and F.A.W. Wilson, and their collaboration is sincerely acknowledged. Some of the research described was supported by the Medical Research Council, PG8513790 and
References (146)
Organization of cortical afferent input to the orbitofrontal area in the rhesus monkey
Neuroscience
(1993)Anatomic basis of cognitive–emotional interactions in the primate prefrontal cortex
Neuroscience and Biobehavioural Reviews
(1995)- et al.
Responses of neurons in the primate taste cortex to glutamate
Physiology and Behavior
(1991) - et al.
Insensitivity to future consequences following damage to human prefrontal cortex
Cognition
(1994) Perseveration in extinction and in discrimination reversal tasks following selective prefrontal ablations in Macaca mulatta
Physiology and Behavior
(1969)- et al.
The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey
Behavioural Brain Research
(1989) - et al.
Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage
Neuropsychologia
(1996) - et al.
Projections from behaviorally defined sectors of the prefrontal cortex to the basal ganglia, septum and diencephalon of the monkey
Experimental Neurology
(1968) - et al.
Limbic lesions and the problem of stimulus–reinforcement associations
Experimental Neurology
(1972) - et al.
Olfactory identification in patients with focal cerebral excision
Neuropsychologia
(1988)
The role of the inferior prefrontal convexity in performance of delayed nonmatching-to-sample
Neuropsychologia
Neural correlates of rapid reversal learning in a simple model of human social interaction
Neuroimage
Effects of satiety on self-stimulation of the orbitofrontal cortex in the monkey
Neuroscience Letters
An electrophysiological and behavioural study of self-stimulation in the orbitofrontal cortex of the rhesus monkey
Brain Research Bulletin
Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta)
Brain Research
Brain mechanisms for invariant visual recognition and learning
Behavioural Processes
Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition
Neuron
The Hebbian paradigm reintegrated: Local reverberations as internal representations
Behavioural and Brain Sciences
Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey
Journal of Comparative Neurology
Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey
Journal of Computational Neurology
Amygdalectomy and ventromedial prefrontal ablation produce similar deficits in food choice and in simple object discrimination learning for an unseen reward
Experimental Brain Research
Afferent connections of the orbitofrontal cortex taste area of the primate
Neuroscience
Deciding advantageously before knowing the advantageous strategy
Science
Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex
Cerebral Cortex
Borderline personality disorder, impulsivity and the orbitofrontal cortex
Biological Psychiatry
View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex
Cerebral Cortex
Face-selective neurons in the primate orbitofrontal cortex
Society for Neuroscience Abstracts
Orality, preference behavior, and reinforcement value of non-food objects in monkeys with orbital frontal lesions
Science
Alterations in aversive and aggressive behaviors following orbitofrontal lesions in rhesus monkeys
Acta Neurobiologiae Experimentalis
Effects of orbitofrontal lesions on aversive and aggressive behaviors in rhesus monkeys
Journal of Comparative and Physiological Psychology
Central olfactory connections in the macaque monkey
Journal of Comparative Neurology
Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey
Journal of Comparative Neurology
Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys
Journal of Comparative Neurology
Olfactory neuronal responses in the primate orbitofrontal cortex: Analysis in an olfactory discrimination task
Journal of Neurophysiology
Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex
Journal of Neurophysiology
Responses of primate taste cortex neurons to the astringent tastant tannic acid
Chemical Senses
Orbitofrontal cortex responses to the texture, taste, smell and sight of food
Appetite
Descartes' error
Representation of umami taste in the human brain
Journal of Neurophysiology
Human cortical responses to water in the mouth, and the effects of thirst
Journal of Neurophysiology
Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain
European Journal of Neuroscience
Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex
European Journal of Neuroscience
Neural mechanisms for visual memory and their role in attention
Proceedings of the National Academy of Sciences USA
Behavioral effects of selective ablation of the caudate nucleus
Journal of Comparative Physiological Psychology
The representation of pleasant touch in the brain and its relationship with taste and olfactory areas
NeuroReport
Psychosurgery in the treatment of mental disorders and intractable pain
Mnemonic coding of visual space in monkey dorsolateral prefrontal cortex
Journal of Neurophysiology
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