The orbitofrontal cortex and beyond: From affect to decision-making
Introduction
The functions of the orbitofrontal cortex and how it relates to areas to which it is connected are considered here, based on its connections, neurophysiology, activation in functional neuroimaging studies, and on the effects of damage to the orbitofrontal cortex. Activity in the orbitofrontal cortex is compared to that in the areas that project to it, and to the activity in the areas to which it projects. This enables us to develop a theme of how sensory representations in the input regions are transformed into reward-related representations in the orbitofrontal cortex important in affective value and emotion, and then to representations used to make decisions (choices) based on reward value in areas beyond the orbitofrontal cortex to which it projects. We also describe new evidence for how top-down cognitive and attentional inputs coming from beyond the orbitofrontal cortex to the orbitofrontal cortex can influence the affective representations in the orbitofrontal cortex, showing how cognition descends down into the emotional system in the brain to influence what we feel.
The focus is on humans and macaques, because there are many topological, cytoarchitectural, and probably connectional similarities between macaques and humans with respect to the orbitofrontal cortex (see Fig. 1 and Carmichael and Price, 1994, Kringelbach and Rolls, 2004, Öngür and Price, 2000, Petrides and Pandya, 1995, Price, 2006, Price, 2007). This brain region may be less well developed in rodents. Moreover, the orbitofrontal cortex receives visual information in primates from the inferior temporal visual cortex, which is a highly developed area for primate vision enabling invariant visual object recognition (Rolls, 2000a, Rolls, 2007c, Rolls, 2008e, Rolls and Deco, 2002, Rolls and Stringer, 2006), and which provides visual inputs used in the primate orbitofrontal cortex for one-trial object-reward association reversal learning, and for representing face expression and identity. Further, even the taste system of primates and rodents may be different, with obligatory processing from the nucleus of the solitary tract via the thalamus to the cortex in primates, but a subcortical pathway in rodents via a pontine taste area to the amygdala, and differences in where satiety influences taste responsive neurons in primates and rodents (Norgren, 1984, Rolls, 2005, Rolls and Scott, 2003). To understand the functions of the orbitofrontal cortex in humans, the majority of the studies described here were therefore performed with macaques or with humans.
Evidence from the connections, effects of damage, single neuron recording, functional neuroimaging, and computational neuroscience is all necessary in order to understand cortical function, and evidence from all these approaches is included in this review. Single neuron responses are essential for understanding the nature of the representation in a cortical area, for each neuron contributes in a different way to the ensemble encoding of stimuli, with each neuron having a different profile of tuning to a subset of the stimuli to provide high capacity and good generalization (see examples in Fig. 3, Fig. 5), and the properties of exactly what is represented (such as which aspects of taste, texture, smell, face, touch, etc. are independently represented) only being measurable by comparing the responses of single neurons (Rolls, 2008e). The use of information theory to determine what is represented by neurons about stimuli or events in the world by using the mutual information between the stimuli and the neuronal responses is a rigorous way to analyse this, as has been described elsewhere (Rolls, 2008e), and shows that most of the information in the responses of neurons in cortical areas during behaviour and with attention is carried by the number of spikes in a short interval of 20–50 ms, rather than by any stimulus-dependent synchronization or temporal encoding (Aggelopoulos et al., 2005, Rolls, 2008e: Appendix on information theory and neuronal encoding). Evidence at this neuronal level is needed to provide the basis for computational theories of brain function, which need to specify what is encoded by the computing elements of the brain between which information is exchanged, the neurons (Rolls, 2008e). Functional neuroimaging studies are valuable for allowing aspects of human brain function to be analysed, including for example some of the top-down effects of attention and cognition on sensory and reward processing that are described below.
Section snippets
Connections
Part of the background for understanding neuronal responses in the orbitofrontal cortex is the anatomical connections of the orbitofrontal cortex (Barbas, 1995, Carmichael and Price, 1994, Carmichael and Price, 1995, Öngür and Price, 2000, Pandya and Yeterian, 1996, Petrides and Pandya, 1995, Price, 2006, Price, 2007). A schematic diagram that helps to show the stage of processing in different sensory streams of the orbitofrontal cortex is provided in Fig. 2. Conceptually, the orbitofrontal
Effects of damage to the orbitofrontal cortex
Part of the evidence on the functions of the orbitofrontal cortex comes from the effect of lesions of the orbitofrontal cortex. Macaques with lesions of the orbitofrontal cortex are impaired at tasks that involve learning about which stimuli are rewarding and which are not, and are especially impaired at 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
Taste: a primary reinforcer
One of the discoveries that have helped us to understand the functions of the orbitofrontal cortex in behaviour is that it contains a major cortical representation of taste (see Kadohisa et al., 2005, Rolls, 1995, Rolls, 1997, Rolls and Scott, 2003, Rolls et al., 1990) (cf. Fig. 2). Given that taste can act as a primary reinforcer, that is without learning as a reward or punisher, we now have the start for a fundamental understanding of the function of the orbitofrontal cortex in
Somatosensory and temperature inputs to the orbitofrontal cortex, and affective value
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 (Francis et al., 1999, Rolls et al., 2003b).
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Visual inputs to the orbitofrontal cortex, visual stimulus-reinforcement association learning and reversal, and negative reward prediction error neurons
We have been able to show that there is a major visual input to many neurons in the orbitofrontal cortex, and that what is represented by these neurons is in many cases the reinforcement association of visual stimuli. The visual input is from the ventral, temporal lobe, visual stream concerned with “what” object is being seen (see Rolls, 2000a, Rolls and Deco, 2002). Many neurons in these temporal cortex visual areas have responses to objects or faces that are invariant with respect to size,
Face-selective processing in the orbitofrontal cortex
Another type of visual information represented in the orbitofrontal cortex is information about faces. There is a population of orbitofrontal neurons that respond in many ways similar to those in the temporal cortical visual areas (Rolls, 1984, Rolls, 1992, Rolls, 1996, Rolls, 2000a, Rolls, 2007c, Rolls, 2008c, Rolls, 2008e, Rolls and Deco, 2002). The orbitofrontal face-responsive neurons, first observed by Thorpe et al. (1983), then by Rolls et al. (2006), tend to respond with longer latencies
Top-down effects of cognition and attention on taste, olfactory, flavor, somatosensory, and visual processing: cognitive enhancement of the value of affective stimuli
How does cognition influence affective value? How does cognition influence the way that we feel emotionally? Do cognition and emotion interact in regions that are high in the brain’s hierarchy of processing, or do cognitive influences descend down to influence the first regions that represent the affective value of stimuli?
An fMRI study to address these fundamental issues in brain design has shown that cognitive effects can reach down into the human orbitofrontal cortex and influence
Emotion and the orbitofrontal cortex
From earlier approaches (Gray, 1975, Millenson, 1967, Weiskrantz, 1968), Rolls has developed the theory over a series of stages that emotions are states elicited by instrumental reinforcers1 (
Individual differences in emotion, and the orbitofrontal cortex
Given that there are individual differences in emotion, can these individual differences be related to the functioning of brain systems involved in affective behaviour such as the orbitofrontal and pregenual cingulate cortex?
Some individuals, chocolate cravers, report that they crave chocolate more than non-cravers, and this is associated with increased liking of chocolate, increased wanting of chocolate, and eating chocolate more frequently than non-cravers (Rodriguez et al., 2007). In a test
A representation of novel visual stimuli in the orbitofrontal cortex
A population of neurons has been discovered in the primate orbitofrontal cortex that responds to novel but not familiar visual stimuli, and takes typically a few trials to habituate (Rolls et al., 2005). The memories of these neurons last for at least 24 h. Exactly what role these neurons have in memory is not yet known, but there are connections from the area in which these neurons are recorded to the temporal lobe, and activations in a corresponding orbitofrontal cortex area in humans are
Beyond the orbitofrontal cortex to choice decision-making
In the neurophysiological studies described above, we have found that neuronal activity is related to the reward value of sensory stimuli, and how these change when reward contingencies change, but is not related to the details of actions that are being performed, such as mouth or arm movements (Rolls, 2005, Rolls, 2008e). Wallis (2007) and Padoa-Schioppa and Assad (2006) have obtained evidence that supports this. An implication is that the orbitofrontal cortex represents the reward, affective
A computational basis for stimulus-reinforcer association learning and reversal in the orbitofrontal cortex involving conditional reward neurons and negative reward prediction error neurons
The neurophysiological, imaging, and lesion evidence described above 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. In addition, it has been shown that amphetamine, a potent instrumental reinforcer, is self-administered to the orbitofrontal cortex by macaques (Phillips et al., 1981), and that in drug naïve human
Representations of affective value vs. intensity and identity
An important principle that emerges from research on the brain mechanisms of emotion is that there is a specialized system that provides representations of the reward or reinforcing value of stimuli, and that this is separate from brain systems that represent the physical properties of a stimulus such as its identity (e.g., that it is sweet, independently of hunger and whether we want it and it is currently rewarding; what object we are looking at, independently of whether we want it and it is
Acknowledgements
The authors have worked on some of the experiments described here with I. Araujo, G.C. Baylis, L.L. Baylis, A. Bilderbeck, R. Bowtell, A.D. Browning, H.D. Critchley, S. Francis, M.E. Hasselmo, J. Hornak, M. Kadohisa, M. Kringelbach, C.M. Leonard, C. Margot, C. McCabe, F. McGlone, F. Mora, J. O’Doherty, B.A. Parris, D.I. Perrett, T.R. Scott, S.J. Thorpe, M.I. Velazco, J.V. Verhagen, E.A. Wakeman and F.A.W. Wilson, and their collaboration is sincerely acknowledged. Some of the research described
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