Keywords: orbitofrontal, sensory qualia, sub-cortical structures, limbic structures
The papers in this book deal most of all with the links between the orbitofrontal cortex and the amygdala plus other parts of the limbic system that instantiate emotional processing in the brain. There is scant mention of consciousness, qualia or how these relate to emotional experience. However, it would seem that this is in fact of central importance to the brain processes discussed. In one sense, emotions are a ‘purer’ form of qualia than the sensory qualia, such as the colour red, because a colour can be equated to a particular frequency of light. By contrast, it is not possible to obtain a comparable reading for an emotion, for say the fear of crocodiles.
Emotion is also important in the consciousness debate, in that it is what we might use to determine whether another entity capable of purposeful action, say a robot or an alien, was conscious or not. This is because in humans, and probably more advanced animals, emotions lie behind our preferences for one course of action over another. This is brought very much to the fore by several of the papers in this volume, which emphasise the connection between the preference evaluating orbitofrontal cortex and the emotional processing of the amygdala and other limbic structures. The combined efforts of these two brain regions are crucial to goal-directed behaviour and social interaction. Patients who have lesions in the orbitofrontal have pronounced problems with both goal-directed activity and appropriate social interaction.
Chapter 4: Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex
Helen Barbas & Basil Zikopoulos
The prefrontal cortex guides behaviour by drawing information from both the cortex and sub-cortical structures. In addition to this, the orbitofrontal and medial sectors of the prefrontal have strong connections with the structures that process emotions. The three prefrontal areas of the brain, the lateral, the orbitofrontal and the medial areas are interconnected, and are involved in the interaction of cognitive and emotional processes. The integration of cognitive and emotional areas is seen as particularly important, and it is known that disruption of this link has a serious effect on behaviour.
Decisions and actions are seen as being inextricably linked to the emotional impact of events. The orbitofrontal is particularly important in this respect. Orbitofrontal damage results in deficits in emotional responses and social interaction. The orbitofrontal’s connections with temporal lobe structures suggest that it conveys signals related to the emotional significance of events. There are strong connections between the orbitofrontal and the perihinal region of the temporal lobe. Both the orbitofrontal and the perihinal have multimodal connections. The orbitofrontal receives projections from the auditory, somatosensory and other association cortex, and can sample the entire sensory range. The orbitofrontal also receives projections from cortical limbic areas, such as the medial temporal lobe and the cingulate cortex, which are thought to provide information about the internal environment of the body. There are also strong connections with the amygdala and the limbic thalamus. The orbitofrontal is here seen as an integrator of information from the external and internal environments, and it is suggested that such integration is necessary for signalling the emotional significance of events.
Sensory input reaches the orbitofrontal by means of projections from the sensory association cortices and indirectly through the amygdala that also receives projections from the sensory association cortices. The connections between the orbitofrontal and the amygdala are strong and work in both directions. There is a large overlap between the parts of the association cortices projecting to the orbitofrontal and those projecting to the amygdala. This is demonstrated to be a triangular structure involving association cortex, orbitofrontal and amygdala. This is suggested to be involved in processing the emotional significance of events. This can have related significance for motivational drives, and the system is involved in remembering behaviour that is rewarded and rejecting it, if it ceases to be rewarded. Reward expectancy is based on information from the sensory association cortex, and both the orbitofrontal and the amygdala are activated in relation to the expectation and detection of reward. Circuitry linking midbrain dopamine producing neurons, the amygdala and the orbitofrontal is involved in the experience of reward and subsequent behavioural changes.
Projections from the orbitofrontal to the amygdala have the effect of reducing the latter’s inhibitory output to the autonomic centres in the hypothalamus and the brainstem. The orbitofrontal can thus allow or inhibit the hypothalamic and brainstem influences on the body. The orbitofrontal and the amygdala are suggested to act together on the hypothalamus and the brainstem. All these connections are viewed as being activated when an event has emotional significance, and particularly when this involves a sense of danger. Separate pathways between the orbitofrontal and the amygdala handle excitatory and inhibitory signals. These systems are viewed as underlying the processing of emotional behaviour. Experiments suggest that the interaction between the orbitofrontal and the amygdala is necessary for consciousness of emotion. Conditioned fear has been shown to be supported by a sub-cortical loop between the thalamus and the amygdala. The amygdala is connected to other limbic structures involved with the processing of the internal environment. It is involved in rapid and mainly unconscious processing of this material, although it is suggested to be poised to direct attention to anything that is sufficiently important.
Studies indicate that the involvement of the cortex is necessary for consciousness of emotions. This is seen as being a function of the connections between the orbitofrontal and the sensory association cortices. Direct sensory input to the orbitofrontal may provide a picture of the external environment, while the amygdala may provide the emotional colouring to allow the interpretation of this picture. This in turn may result in the activation of autonomic structures. The orbitofrontal also has connections with structures associated with the formation of long-term memories, notably the entorhinal cortex, which is strongly connected to the hippocampus. The orbitofontal is thought to give signals to the entorhinal as to the emotional significance of events. The orbitofrontal can also distinguish between current input and irrelevant memories. Information received from sensory areas may be processed in the orbitofrontal before being signalled to the hippocampus. In the opposite direction learning systems in the hippocampus project direct to the orbitofrontal to indicate where rewards are found in the external environment. An interconnected network of the amygdala, the orbitofrontal and the mediodorsal nucleus in the thalamus may underlie the processing of emotionally significant events into the long-term memory. Another circuit associated with long-term memory involves the amygdala, the orbitofrontal and the anterior medial nucleus in the thalamic limbic nuclei. This links the orbitofrontal and the anterior cingulate with systems underlying long-term memory. Damage to the anterior medial is associated with impairment to long-term memory. The anterior medial is also associated with the processing of emotions and receives projections from the amygdala. The orbitofrontal receives numerous projections from the limbic thalamic nuclei.
Recent evidence suggests that circuits passing through the basal ganglia are involved in cognition, reward evaluation, motivated behaviour, learning and memory, and that these circuits may be traced to the prefrontal cortex. The ventral anterior is among the thalamic nuclei projecting to the prefrontal cortex, and its connections with the medial and orbitofrontal cortex are seen as important for motivational and emotional processing. The orbitofrontal is suggested to collaborate with other areas of the prefrontal in forming decisions. The orbitofrontal and medial prefrontal are suggested to have complementary roles in emotional processing, with the medial responding most of all to autonomic material.
This chapter points out the strong connection between the orbitofrontal and limbic structures that process emotions. It refers in particular to the interconnection of cognition and emotional processing. Although mainstream thinking has worked to marginalise or eliminate consciousness from much role in brain function, when it comes to the practical day-to-day processes described in this paper, it is admitted that cognition is entwined with the undeniably conscious experience of emotion. It is stressed that any disruption of the link between cortical processing and conscious emotions leads to deficits in behaviour. Decision taking in particular is linked to the conscious emotions.
Chapter 7: Involvement of orbitofontal neurons in reward, uncertainty and learning
Wolfram Schultz, University of Cambridge
& Leon Tremblay, Hopital de la Salpetriere, Paris
Orbitofrontal functions are related to emotional processing that underlies responses to the environment. This is particularly true of responses to rewards for particular actions. The neurons also appear to code the value of a reward, and not just whether or not it will be received. Survival in many environments requires responsiveness to numerous different reward objects. Rewards can be ranked according to their value. Such values are not fixed like physical properties, but fluctuate according to availability and satiety. So carrots might be the most preferred item if only carrots and apples are available, but bananas could take over this top slot, if they suddenly become available alongside carrots and apples. What the neurons respond to are the order of preference, not the physical object itself.
The orbitofrontal appears to be one of the main reward centres in the brain, together with the dorsal and ventral striatum and the dopamine neurons. Alongside the orbitofrontal, the striatal neurons are involved in processing reward information. It is speculated that orbitofrontal inputs could provide motivational information to the dorsolateral prefrontal with respect to rewards and punishments. It is suggested the orbitofrontal is not restricted to monitoring the current external world, but can also possess representations of the outside world, so that it can anticipate future rewards. These inner representations change over time in response to the actual experience of reward or non-reward.
The orbitofrontal is thought to encode the relative values of rewards that a human or an animal might be able to achieve. The response is not to the physical object but to its relative value within a series of choices. So if carrots and apples are offered, carrots might be preferred and the top preference signal in the brain would equate to these. However, if the choice was extended so as to include bananas, carrots and apples, the top preference signal could be switched to equate to bananas. This looks hard to equate in terms of a one-to-one relationship with visual signals from physical objects, but looks to require the previous experience or qualia of having eaten bananas.
Chapter 8: The orbitofrontal as the gateway between the limbic system and the representational memory
Matthew Roesch & Geoffrey Schoenbaum
University of Maryland, School of Medicine
The orbitofrontal has connections to the autonomic musculature and the endocrine systems. It is involved in emotional learning within in a circuit that includes the amygdala and other limbic structures. The authors argue that the structure manipulates information about the value of likely outcomes within representational memory. The resultant expectancies are seen as influencing both limbic areas and other prefrontal regions, and thus directing learning, cognition and goal-directed behaviour. The authors think that orbitocortical processing goes beyond simply learning reward/punishment outcomes, and integrates information with current plans and the internal state.
The orbitofrontal is seen as an important link between the emotional processing of the limbic system and the representational memory systems of the prefrontal. It is well placed to integrate information regarding planned actions. Orbitofrontal neurons appear to fire in relation to the value of predicted outcomes, with the response relating to the meaning of the stimuli, rather than its actual physical properties.
Responses in the orbitofrontal tend to reflect a judgement, such as what consequences will follow on a particular action, given the current circumstances. In different circumstances, there could be a different response to the same physical object. The orbitofrontal response is viewed as reflecting the expected value of the subsequent state given a particular response. This involves an internalised model of a future reality. The subsequent outcome can then can be compared to previously represented expectation. This view has been supported by recent studies. Firing relative to rewards appears to take into account aspects such as the time required to obtain the reward and the consequences of alternative behaviour. The importance of the orbitofrontal is highlighted by the consequences of damage in this area, which results particularly in a reduction in inhibitions against inappropriate or reckless actions. This is viewed as a consequence of lack of representations of the possible consequences of actions. There is also an inability to alter behaviour, when it should have been possible to learn that a particular course of action was having adverse consequences. The ability of the orbitofrontal to predict the likely consequences of actions can be used by other brain regions to guide behaviour.
Chapter 9: A componential analysis of the functions of the orbitofrontal
Angela Roberts, Dept. of Psychology, University of Cambridge
& John Parkinson, University of Wales
Studies show that neurons in the orbitofrontal signal the expected outcomes of actions based on past experience. The orbitofrontal is shown to be encoded as a result of behaviour, while the amygdala is encoded before behaviour. The orbitofrontal is seen as being capable of creating a common neural currency that can weigh up not directly comparable rewards such as food, money and sex. It is thought to be capable of an explicit expectancy based value judgement. The choosing process in the orbitofrontal is suggested to involve the inhibition or suppression of some alternative choices. It is hard to see what medium the neural currency could use other than that of conscious emotional satisfaction or dissatisfaction. It is possible to equate the value of a particular meal with £100, but this depends on comparing the conscious experience of a meal like the one expected, and the conscious experience of being £100 worse off than one was before. This implies that contrary to much mainstream philosophising conscious emotions must play an active role in brain functions.
Chapter 10: John Doherty & Raymond Dolan
The orbitofrontal is highly connected both with sub-cortical structures such as the amygdala, the ventral and dorsal striatums and the dopamine producing neurons in the midbrain, as well as other parts of the prefrontal cortex. The orbitofrontal is demonstrated to assess subjective measures of rewards such as degrees of pleasantness, and can also assess abstract rewards such as money or social approval. Different types of reward are also somehow encoded in a common neural currency, the implications of which were discussed at the end of the previous chapter. Some adaptive behaviour is selected on the basis of immediate outcome. In other cases, it is advantageous to assess outcomes of varying probability and varying magnitude. For this, it is necessary to calculate the future reward for a particular action. Neuroimaging studies have indicated the involvement of the orbitofrontal, the amygdala and the ventral striatum in reward prediction. Studies show that it was the reward values, rather than the physical properties of objects, that were coded in the orbitofrontal. Results of studies suggest that the orbitofrontal both signals predictions of rewards, and also compares the prediction to what is actually received. One view is that the amygdala codes for the intensity of a stimulus and the orbitofrontal for its value. The orbitofrontal is seen as contributing to the flexibility of responses by monitoring the achievement of rewards, and errors in obtaining rewards.
Chapter 11: Memory and the orbitofrontal
Matthias Brand & Hans Markowitsch
Dept. of Physiological Psychology, University of Bielefeld
The orbitofrontal is viewed as being involved in autobiographical memory that is of emotional and personal significance Autobiographical memory is defined as episodic memory (recall of events including time and place, emotional tone and sense of self), plus the mundane facts of autobiography, such as name and address. The orbitofrontal is strongly connected with structures in the limbic system. Current thinking on emotion favours the importance of the amygdaloid circuit over the more traditional definitions of the limbic. The amygdaloid circuit includes the amygdala, the mediodorsal nucleus in the thalamus, parts of the basal forebrain and several interconnecting fibres.
The orbitofrontal is heavily connected with the limbic structures most involved in the processing of emotions. It is the part of the prefrontal most involved in emotional processing, and therefore likely to be involved in emotional memory. Some authors regard it as an expanded part of the limbic system. The connection with the anterior temporal pole is seen as important. This is involved in the retrieval of both episodic memory and facts. A number of interacting brain regions are engaged in the retrieval of episodic memory. These include much of the prefrontal and the temporal cortex and the posterior cingulate. Recent studies demonstrate that the orbitofrontal is important for adjusting thoughts and behaviour to current stimuli, and in selecting memories of current relevance. It is seen as having a role in the mediation of specific memories and the memory related emotions.
Chapter 13: Visceral and decision making functions
Nasir Naqvi, Daniel Tranel & Antoine Bechara
Dept. of Neurology, University of Iowa
Studies show that damage to the ventromedial prefrontal cortex (VMPFC) at the junction of the orbitoprefrontal and mesial prefrontal can lead to problems with patients’ ability to take advantageous decisions. This is related to the ‘somatic marker hypothesis’ of Damasio. He argued that patients with lesions in this area made poor decisions, because they were unable to receive bodily or visceral responses that mark the consequences of their actions as positive or negative. The VMPFC is seen as functioning to obtain visceral responses that reflect the anticipated value of choices that the subject could make. Studies show that patients with VMPFC damage are impaired in their visceral response to emotional pictures.
Brains differ from computers in, amongst other things, needing to promote survival by regulating the internal state of the body. For this reason, nervous systems contain representations of bodily processes in order to maintain the state of the body within the ranges that are essential for life (homeostasis). The autonomic nervous system makes rapid adjustments to achieve this end. A further survival advantage comes from the ability to predict the impact of events on the internal state. The somatic marker hypothesis suggests that the VMPFC plays a part in integrating the viscera with processes of perception, learning, memory and goal-directed behaviour. This is related to the planning of behaviour for the future, and outcomes expressed in abstract terms.
Chapter 15: Orbital cortex activation during studies of emotion
Darin Dougherty, Lisa Shin & Scott Rauch
Dept. of Psychiatry, Massachusetts Gen. Hospital
Recent theorists have suggested that three components are essential for emotional perception; identification of the emotional significance of a stimulus, the production of an emotional state, and the regulation of the emotional state. The amygdala is identified as the first-line processor of emotional information. The regulation of emotional states involves the neocortical brain regions. There is reduced activity in the ventral prefrontal, when the dorsolateral prefrontal is activated during cognitive tasks. It is thought possible that the orbitofontal responds to dorsal activity by dampening the autonomic responses, which were the initial emotional response. Orbitofrontal activation happens shortly after the response by the amygdala. The amygdala and the orbitofrontal are central to the generation of autonomic responses. The somatic marker hypothesis suggests that the resulting autonomic state alerts the body, and produces a conscious emotional state. The emotional state produced causes the brain to respond to stimuli in an adaptive manner.