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
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