Scientific Understanding of Consciousness
Orbitofrontal Cortex Functions
Brain and Cognition 55 (2004) 11–29
Functions of the Orbitofrontal Cortex
Edmund T. Rolls
Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, England, UK
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 association of the visual stimulus with a primary reinforcing stimulus (such as taste) is reversed. This is an example of stimulus–reinforcement association learning, and is a type of stimulus–stimulus association learning. More generally, the stimulus might be a visual or olfactory stimulus, and the primary (unlearned) positive or negative reinforcer a taste or touch. A somatosensory input is revealed by neurons that respond to the texture of food in the mouth, including a population that responds to the mouth feel of fat. In complementary neuroimaging studies in humans, it is being found that areas of the orbitofrontal cortex are activated by pleasant touch, by painful touch, by taste, by smell, and by more abstract reinforcers such as winning or losing money. Damage to the orbitofrontal cortex can impair the learning and reversal of stimulus–reinforcement associations, and thus the correction of behavioural responses when there are no longer appropriate because previous reinforcement contingencies change. The information which reaches the orbitofrontal cortex for these functions includes information about faces, and damage to the orbitofrontal cortex can impair face (and voice) expression identification. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behavior, and thus in emotion. The approach described here is aimed at providing a fundamental understanding of how the orbitofrontal cortex actually functions, and thus in how it is involved in motivational behavior such as feeding and drinking, in emotional behavior, and in social behavior.
Prefrontal Cortex is defined by projections from the Thalamus
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 classified into three main regions. First, the magnocellular, medial, part of the mediodorsal nucleus projects to the orbital (ventral) surface of the prefrontal cortex (which includes area 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. 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.
Connections to the Orbitofrontal Cortex
The functions of the orbitofrontal cortex are considered here. 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. 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. Researchers (1990) discovered a taste area in the lateral part of the orbitofrontal cortex, and showed that this was the secondary taste cortex, which receives a major projection from the primary taste cortex The caudal orbitofrontal cortex receives strong inputs from the amygdala. The orbitofrontal cortex also receives inputs via the mediodorsal nucleus of the thalamus, pars magnocellularis, which itself receives afferents from temporal lobe structures such as the prepyriform (olfactory) cortex, amygdala, and inferior temporal cortex. The orbitofrontal cortex projects back to temporal lobe areas such as the inferior temporal cortex. The orbitofrontal cortex has projections to the entorhinal cortex (or ‘‘gateway to the hippocampus’’), and cingulate cortex. The orbitofrontal cortex also projects to the preoptic region and lateral hypothalamus, to the ventral tegmental area.
Macaques as a Model System
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. Lesions more laterally, in for example the inferior convexity, can influence tasks in which objects must be remembered for short periods, e.g., delayed matching to sample and delayed matching to non-sample tasks, and neurons in this region may help to implement this visual object short term memory by holding the representation active during the delay period. It should be noted that this short-term memory system for objects (which receives inputs from the temporal lobe visual cortical areas in which objects are represented) is different from the short-term memory system in the dorsolateral part of the prefrontal cortex, which is concerned with spatial short term memories, consistent with its inputs from the parietal cortex.
Taste can act as a Primary Reinforcer of Behavior
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. 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 learning. We know how one class of primary reinforcers reaches and is represented in the orbitofrontal cortex. A representation of primary reinforcers is essential for a system that is involved in learning associations between previously neutral stimuli and primary reinforcers, e.g., between the sight of an object, and its taste. The representation (shown by analysing the responses of single neurons in macaques) of taste in the orbitofrontal cortex includes robust representations of the prototypical tastes sweet, salt, bitter, and sour, of protein or umami as exemplified by monosodium glutamate, and inosine monophosphate, and of astringency as exemplified by tannic acid. The nature of the representation of taste in the orbitofrontal cortex is that the reward value of the taste is represented. The evidence for this is that the responses of orbitofrontal taste neurons are modulated by hunger (as is the reward value or palatability of a taste). In particular, it has been shown that orbitofrontal cortex taste neurons stop responding to the taste of a food with which the monkey is fed to satiety. In contrast, the representation of taste in the primary taste cortex is not modulated by hunger. Thus in the primate primary taste cortex, the reward value of taste is not represented, and instead the identity of the taste is represented. Additional evidence that the reward value of food is represented in the orbitofrontal cortex is that monkeys work for electrical stimulation of this brain region if they are hungry, but not if they are satiated. Further, neurons in the orbitofrontal cortex are activated from many brain-stimulation reward sites. Thus there is clear evidence that it is the reward value of taste that is represented in the orbitofrontal cortex. The secondary taste cortex is in the caudolateral part of the orbitofrontal cortex, as defined anatomically. This region projects onto other regions in the orbitofrontal cortex, and neurons with taste responses (in what can be considered as a tertiary gustatory cortical area) can be found in many regions of the orbitofrontal cortex. In human neuroimaging experiments (e.g., with functional magnetic resonance image, fMRI), it has been shown (corresponding to the findings in non-human primate single neuron neurophysiology) that there is an orbitofrontal cortex area activated by sweet taste (glucose), and that there are at least partly separate areas activated by the aversive taste of saline (NaCl, 0.1 M) by pleasant touch, and by pleasant vs aversive olfactory stimuli.
Gustatory and Olfactory stimuli Converge in Orbitofrontal Cortex
In these further parts of the orbitofrontal cortex, not only unimodal taste neurons, but also unimodal olfactory neurons are found. In addition some single neurons respond to both gustatory and olfactory stimuli, often with correspondence between the two modalities. It is probably here in the orbitofrontal cortex of primates that these two modalities converge to produce the representation of flavor. Evidence will soon be described that indicates that these representations are built by olfactory–gustatory association learning, an example of stimulus–reinforcement association learning.
A ventral frontal region has been implicated in olfactory processing in humans. Researchers have analyzed the functionality by which orbitofrontal olfactory representations are formed and operate in primates. For 65% of neurons in orbitofrontal olfactory areas, the representation of the olfactory stimulus is independent of its association with taste reward. For the remaining 35% of the neurons, the odors to which a neuron responds is influenced by the taste (glucose or saline) with which the odor is associated. Thus the odor representation for 35% of orbitofrontal neurons appears to be formed by olfactory-to-taste association learning.
Research Study — Olfactory Perception of Odor Molecules from Chemical Features
Visual inputs to the Orbitofrontal Cortex
Researchers have shown that there is a major visual input to many neurons in the orbitofrontal cortex, and that what is represented by these neurons in many cases is the reinforcement association of visual stimuli. The visual input is from the ventral, temporal lobe, visual stream concerned with ‘‘what’’ object is being seen. The primary reinforcer that has been used in the research experiments is taste.
The probable mechanism for this learning is Hebbian modification of synapses conveying visual input onto taste-responsive neurons, implementing a pattern association network. Similar neurons are present for punishing primary reinforcers, such as the aversive taste of salt.
In addition to these neurons that encode the reward association of visual stimuli, other neurons in the orbitofrontal cortex detect non-reward, in that they respond when an expected reward is not obtained. The presence of these neurons is fully consistent with the hypothesis that they are part of the mechanism by which the orbitofrontal cortex enables very rapid reversal of behaviour by stimulus–reinforcement association relearning when the association of stimuli with reinforcers is altered or reversed.
The finding that different orbitofrontal cortex neurons respond to different types of non-reward (Thorpe et al., 1983), may provide part of the brain’s mechanism that enables task or context-specific reversal to occur.
Information about Faces
Another type of information represented in the orbitofrontal cortex is information about faces. There is a population of orbitofrontal neurons which respond in many ways similar to those in the temporal cortical visual areas. The orbitofrontal face-responsive neurons tend to respond with longer latencies than temporal lobe neurons (140–200 ms typically, compared to 80–100 ms). They also convey information about which face is being seen, by having different responses to different faces and are typically harder to activate strongly than temporal cortical face-selective neurons. Many of them respond much better to real faces than to two-dimensional images of faces on a video monitor.
Orbitofrontal Neurons respond to Face Gesture or Movement
Some of the orbitofrontal cortex face-selective neurons are responsive to face gesture or movement. The findings are consistent with the likelihood that these neurons are activated via the inputs from the temporal cortical visual areas in which face-selective neurons are found. The significance of the neurons is likely to be related to the fact that faces convey information that is important in social reinforcement in at least two ways that could be implemented by these neurons. The first is that some may encode face expression, which can indicate reinforcement. The second way is that they encode information about which individual is present, which by stimulus–reinforcement association learning is important in evaluating and utilizing learned reinforcing inputs in social situations, e.g., about the current reinforcement value as decoded by stimulus– reinforcement association of a particular individual. Thus in humans, there is a part of the orbitofrontal cortex that responds selectively in relation to face expression specifically when it indicates that behavior should change.
Somatosensory Inputs to the Orbitofrontal Cortex
Some neurons in the macaque orbitofrontal cortex respond to the texture of food in the mouth. Some neurons alter their responses when the texture of a food is modified by adding gelatine or methyl cellulose, or by partially liquefying a solid food such as apple. Another population of orbitofrontal neurons responds when a fatty food such as cream is in the mouth. These neurons can also be activated by pure fat such as glyceryl trioleate, and by nonfat substances with a fat-like texture such as paraffin oil (hydrocarbon) and silicone oil ((Si(CH3)2O)n). These neurons thus provide information by somatosensory pathways that a fatty food is in the mouth These inputs are perceived as pleasant when hungry, because of the utility of ingestion of foods which are likely to contain essential fatty acids and to have a high calorific value. These single-neuron recording studies thus provide clear evidence on the rich sensory representation of oral stimuli, and of their reward value, that is provided in the primate orbitofrontal cortex.
Pleasant or Painful Touch stimuli activate the Orbitofrontal Cortex
In addition to these oral somatosensory inputs to the orbitofrontal cortex, there are also somatosensory inputs from other parts of the body, and indeed an fMRI investigation we have performed in humans indicates that pleasant and painful touch stimuli to the hand produce greater activation of the orbitofrontal cortex relative to the somatosensory cortex than do affectively neutral stimuli.
Rapid Stimulus–Reinforcement Association Learning implemented by Orbitofrontal Cortex
The neurophysiological, imaging, and lesion evidence 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 view-invariant information, and can associate this at the neuronal level with primary reinforcers such as taste, and reverse these associations very rapidly. Another type of stimulus which can be conditioned in this way in the orbitofrontal cortex is olfactory, although here the learning is slower. It is likely that auditory stimuli can be associated with primary reinforcers in the orbitofrontal cortex, though there is less direct evidence of this yet.
Orbitofrontal Signals to Striatum May Influence Behavior
The orbitofrontal cortex also has neurons that detect non-reward, which are likely to be used in behavioural extinction and reversal. They may do this not only by helping to reset the reinforcement association of neurons in the orbitofrontal cortex, but also by sending a signal to the striatum which could be routed by the striatum to produce appropriate behaviours for non-reward. Indeed, it is via this route, the striatal, that the orbitofrontal cortex may directly influence behaviour when the orbitofrontal cortex is decoding reinforcement contingencies in the environment, and is altering behaviour in response to altering reinforcement contingencies.
Rapid Relearning and Alteration of Responses
Decoding the reinforcement value of stimuli, which involves for previously neutral (e.g., visual) stimuli learning their association with a primary reinforcer, often rapidly, and which may involve not only rapid learning but also rapid relearning and alteration of responses when reinforcement contingencies change, is then a function proposed for the orbitofrontal cortex. This way of producing behavioural responses would be important in for example motivational and emotional behaviour. It would be important for example in motivational behaviour such as feeding and drinking by enabling primates to learn rapidly about the food reinforcement to be expected from visual stimuli. This is important, for primates frequently eat more than 100 varieties of food; vision by visual–taste association learning can be used to identify when foods are ripe; and during the course of a meal, the pleasantness of the sight of a food eaten in the meal decreases in a sensory-specific way, a function that is probably implemented by the sensory-specific satiety-related responses of orbitofrontal visual neurons. With respect to emotional behaviour, decoding and rapidly readjusting the reinforcement value of visual signals is likely to be crucial, for emotions can be described as responses elicited by reinforcing signals.
Rapid Learning, a Social Asset for Primates
The ability to perform this learning very rapidly is probably very important in social situations in primates, in which reinforcing stimuli are continually being exchanged, and the reinforcement value of stimuli must be continually updated (relearned), based on the actual reinforcers received and given. Although the functions of the orbitofrontal cortex in implementing the operation of reinforcers such as taste, smell, tactile, and visual stimuli including faces are most understood, in humans the rewards processed in the orbitofrontal cortex include quite general rewards such as working for ‘‘points,’’ as will be described shortly.
Amygdala and Orbitofrontal Cortex may provide some similar functions
Although the amygdala is concerned with some of the same functions as the orbitofrontal cortex, and receives similar inputs, there is evidence that it may function less effectively in the very rapid learning and reversal of stimulus–reinforcement associations, as indicated by the greater difficulty in obtaining reversal from amygdala neurons, and by the greater effect of orbitofrontal lesions in leading to continuing choice of no longer rewarded stimuli. In primates, the necessity for very rapid stimulus–reinforcement re-evaluation, and the development of powerful cortical learning systems, may result in the orbitofrontal cortex effectively taking over this aspect of amygdala functions.
Behavioural Impairments with Frontal Lobe Damage
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. For example, Milner (1963) showed that in the Wisconsin Card Sorting Task (in which cards are to be sorted according to the colour, shape, or number of items on each card depending on whether the examiner says ‘‘right’’ or ‘‘wrong’’ to each placement), frontal patients either had difficulty in determining the first sorting principle, or in shifting to a second principle when required to. Also, in stylus mazes, frontal patients have difficulty in changing direction when a sound indicates that the correct path has been left (Milner, 1982). It is of interest that, in both types of test, frontal patients may be able to verbalize the correct rules, yet may be unable to correct their behavioral sets or strategies appropriately. Some of the personality changes that can follow frontal lobe damage may be related to a similar type of dysfunction. For example, the euphoria, irresponsibility, lack of affect, and lack of concern for the present or future which can follow frontal lobe damage (see Damasio, 1994; Hecaen & Albert, 1978) may also be related to a dysfunction in altering behaviour appropriately in response to a change in reinforcement contingencies. Indeed, in so far as the orbitofrontal cortex is involved in the disconnection of stimulus–reinforcer associations, and such associations are important in learned emotional responses, then it follows that the orbitofrontal cortex is involved in emotional responses by correcting stimulus– reinforcer associations when they become inappropriate.
Spend Money without Concern for the Future
If patients had received brain damage in a road traffic accident, and compensation had been awarded, the patients often tended to spend their money without appropriate concern for the future, sometimes for example buying a very expensive car. Such patients often find it difficult to invest in relationships too, and are sometimes described by their family as having changed personalities, in that they care less about a wide range of factors than before the brain damage.
Orbitofrontal Cortex Involved in Social Behaviour
The suggestion that follows from this and from impairments of patients with circumscribed surgical lesions of the orbitofrontal cortex on a similar behaviour questionnaire is that the orbitofrontal cortex may normally be involved in much social behaviour, and the ability to respond rapidly and appropriately to social reinforcers is of course an important aspect of primate (including human) social behaviour. To investigate the possible significance of face-related inputs to orbitofrontal visual neurons, we also tested the responses of these patients to faces. We included tests of face (and also voice) expression decoding, because these are ways in which the reinforcing quality of individuals is often indicated.
Identification of Facial and Vocal Emotional Expression
Impairments in the identification of facial and vocal emotional expression were demonstrated in a group of patients with ventral frontal lobe damage who had socially inappropriate behaviour. The expression identification impairments could occur independently of perceptual impairments in facial recognition, voice discrimination, or environmental sound recognition. The face and voice expression problems did not necessarily occur together in the same patients, providing an indication of separate processing. The impairment was found on most expressions apart from happy (which as the only positive face expression was relatively easily discriminable from the others), with sad, angry, frightened, and disgusted showing lower identification than surprised and neutral. Poor performance on both expression tests was correlated with the degree of alteration of emotional experience reported by the patients. There was also a strong positive correlation between the degree of altered emotional experience and the severity of the behavioural problems (e.g., disinhibition) found in these patients. A comparison group of patients with brain damage outside the ventral frontal lobe region, without these behavioural problems, was unimpaired on the face expression identification test, was significantly less impaired at vocal expression identification, and reported little subjective emotional change.
Some Topography in the Orbitofrontal Cortex
In current studies patients with face expression decoding problems do not necessarily have impairments at visual discrimination reversal, and vice versa. This is consistent with some topography in the orbitofrontal cortex. Studies are now being performed to obtain evidence of the precise areas of brain damage that give rise to these deficits. The studies are being performed with patients with discrete surgical lesions of the orbitofrontal cortex (performed for example to remove tumors). These studies are valuable in the context that closed head injuries may, although producing demonstrable damage to the orbitofrontal cortex in structural MRI scans, also produce some damage elsewhere. It is being found that bilateral surgically circumscribed lesions (but not usually unilateral) lesions of the orbitofrontal cortex produce deficits in a probabilistic version of a visual discrimination reversal task with monetary reward.
Orbitofrontal Cortex, a special role in Emotional and Motivational Behaviors
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 association of the visual stimulus with a primary reinforcing stimulus (such as taste) is reversed. This is an example of stimulus–reinforcement association learning, and is a type of stimulus–stimulus association learning. More generally, the stimulus might be a visual or olfactory stimulus, and the primary (unlearned) positive or negative reinforcer a taste or touch.
Orbitofrontal Somatosensory Input, Pleasant Touch, Painful Touch
A somatosensory input is revealed by neurons that respond to the texture of food in the mouth, including a population that responds to the mouth feel of fat. In complementary neuroimaging studies in humans, it is being found that areas of the orbitofrontal cortex are activated by pleasant touch, by painful touch, by taste, by smell, and by more abstract reinforcers such as winning or losing money. Damage to the orbitofrontal cortex can impair the learning and reversal of stimulus–reinforcement associations, and thus the correction of behavioural responses when these are no longer appropriate because previous reinforcement contingencies change.
Orbitofrontal Information about Faces
The information which reaches the orbitofrontal cortex for these functions includes information about faces, and damage to the orbitofrontal cortex can impair face (and voice) expression identification. This evidence thus shows that the orbitofrontal cortex is involved in decoding and representing some primary reinforcers such as taste and touch; in learning and reversing associations of visual and other stimuli to these primary reinforcers; and in controlling and correcting reward-related and punishment-related behaviour, and thus in emotion. The approach described here is aimed at providing a fundamental understanding of how the orbitofrontal cortex actually functions, and thus in how it is involved in motivational behavior such as feeding and drinking, in emotional behavior, and in social behavior.
Orbitofrontal Cortex Involved in Behaviors Produced by Rewards and Punishers
A special role of the orbitofrontal cortex in behavior may arise from the fact that it receives outputs from the ends of a number of sensory systems that define ‘‘what’’ stimuli are being presented (as contrasted for example with ‘‘where’’ stimuli are in space). The inputs it receives include taste and somatosensory stimuli, which are prototypical primary reinforcers. This helps to give the orbitofrontal cortex a special role in behaviors produced by rewards and punishers, which happen to encompass in particular emotional and motivational behavior. The particular role that the orbitofrontal cortex implements for these functions is that it decodes the reward (and punishment) value of these primary reinforcers, and also implements a learning mechanism to enable sensory representations of objects (in, e.g., the visual and olfactory sensory modalities) to be associated with these primary reinforcers. Indeed, the orbitofrontal cortex appears to play a special role in such learning, because it can rapidly reverse such stimulus–reinforcement associations. It may be able to perform this reversal more efficiently and rapidly than the amygdala because, as a neocortical structure, its learning mechanisms include rapid and powerful long-term associative synaptic depression (LTD), occurring for example if a visual stimulus represented presynaptically is no longer associated with firing of a post-synaptic neuron responsive to a reward such as sweet taste.
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Orbitofrontal cortex -- inhibits inappropriate actions, allowing us to defer immediate reward in favor of long-term advantage. (Carter; Mapping the Mind, 182)
Orbitofrontal cortex has rich neural connections to the unconscious brain where drives and emotions are generated. The down signals from the cortex inhibit reflex clutching and grabbing. (Carter; Mapping the Mind, 197)
Orbitofrontal cortex appears to be the area of the brain that bestows a quality we may refer to as free will. (Carter; Mapping the Mind, 197)
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