Review
Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex

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Abstract

Emotions are multifaceted, but a key aspect of emotion involves the assessment of the value of environmental stimuli. This article reviews the many psychological representations, including representations of stimulus value, which are formed in the brain during Pavlovian and instrumental conditioning tasks. These representations may be related directly to the functions of cortical and subcortical neural structures. The basolateral amygdala (BLA) appears to be required for a Pavlovian conditioned stimulus (CS) to gain access to the current value of the specific unconditioned stimulus (US) that it predicts, while the central nucleus of the amygdala acts as a controller of brainstem arousal and response systems, and subserves some forms of stimulus–response Pavlovian conditioning. The nucleus accumbens, which appears not to be required for knowledge of the contingency between instrumental actions and their outcomes, nevertheless influences instrumental behaviour strongly by allowing Pavlovian CSs to affect the level of instrumental responding (Pavlovian–instrumental transfer), and is required for the normal ability of animals to choose rewards that are delayed. The prelimbic cortex is required for the detection of instrumental action–outcome contingencies, while insular cortex may allow rats to retrieve the values of specific foods via their sensory properties. The orbitofrontal cortex, like the BLA, may represent aspects of reinforcer value that govern instrumental choice behaviour. Finally, the anterior cingulate cortex, implicated in human disorders of emotion and attention, may have multiple roles in responding to the emotional significance of stimuli and to errors in performance, preventing responding to inappropriate stimuli.

Introduction

Emotions are difficult to define, as the word ‘emotion’ has been applied to a diverse array of perceptions, psychological states and behavioural responses. Human emotions are particularly difficult to consider in the absence of the conscious interpretations that direct and crystallize our feelings and interpretations of emotional experiences. However, it is likely that emotions evolved from simple mechanisms that gave animals the capacity to avoid harm and seek physiologically valuable resources. Consequently, simple and evolutionarily old brain systems may serve fundamental aspects of ‘emotional’ processing, and provide information and motivation for phylogenetically more recent systems to control complex behaviour. In this sense, understanding emotional processing in animals such as rodents and non-human primates can offer insight into the neurobiology of human emotion.

The range of behaviour that has been suggested to reflect emotional states in experimental animals is large. In part, this reflects the difficulty in defining human emotions; for example, while fear has been held to be more specifically directed at a stimulus than anxiety, both have similar symptoms [1], [2]. Therefore, when attempting to analyse emotional behaviour in experimental animals, many neurobiologists have chosen the pragmatic approach of studying a small number of well-defined, learned responses [3]. For example, once a rat has experienced pairings of a simple visual or auditory stimulus with electric shock, it will respond to that stimulus with immobility (freezing). The freezing response has been widely studied as an index of a central fear state [4], [5], [6], [7], and its neural substrate is relatively well understood [8], [9], [3], [10].

In contrast, learning theorists have for many decades addressed emotional learning in a broader sense, asking what information is learned during each task and subsequently represented in the brain, how these representations are formed, and to what uses they are put. Consequently, it is useful to consider under the umbrella of emotion those neural processes by which an animal judges and represents the value of something in the world, and responds accordingly. As will be described later, there are many such processes, and they have different uses. It is becoming increasingly clear that associative learning (including the acquisition of emotional value by a stimulus, context or event) is not a simple or unitary phenomenon. Overt behaviour is determined by the interaction of many learning and memory systems, some complementary, some competitive. Therefore, an understanding of emotion and motivation requires that these systems are recognized and characterized; behavioural neuroscientists face the challenge of teasing apart the contributions of multiple systems to behaviour in order to elucidate their neural mechanisms.

It is not the intention of this review to propose a new model of conditioning or a theory of emotion. Instead, the neural representations that govern two major classes of behaviour, Pavlovian and instrumental conditioned responding, will be considered. Using this psychological framework, the contributions of the amygdala, ventral striatum, and prefrontal cortex (PFC) to emotional and motivated behaviour will be reviewed. In each case, neural systems will be related to the psychological representations to which they appear to correspond.

Section snippets

Psychological basis of emotion and motivation

Associative learning can account for the development of an emotional response. For example, the development of fear can be seen simply as a consequence of the association of an event or stimulus with an unpleasant experience. Such Pavlovian conditioning methods are regularly used to induce stimulus-specific fear in laboratory animals, dating from the time of Bekhterev [11], but are also effective in humans (first shown in Ref. [12]). Can such conditioning fully account for emotional learning?

The amygdala consists of a group of nuclei involved in emotional learning and expression

The amygdala is probably the structure most implicated in emotional processing. Since the demonstration that monkeys with amygdala lesions were ‘fearless’—part of the Klüver–Bucy syndrome [77]—it has been recognized that the amygdala is a key element of the neural basis of emotion. Damage to the amygdala in humans may lead to an increase in threshold of emotional perception and expression [78], [79], [80]; amygdala lesions certainly cause impairments in emotional learning [81], deficits in the

The nucleus accumbens and its associated corticostriatal circuitry

Though the amygdala influences simple, innate behavioural patterns through its projections to the hypothalamus and brainstem, the motivational effects of emotionally significant stimuli are mediated in part by the ventral striatum, specifically the nucleus accumbens (Acb) [170]. While the Acb conforms broadly to the pattern of the cortico-striatal-pallido-thalamo-cortical ‘loop’ typical of the striatum [188], [189], it is a recipient of information from a considerable array of limbic structures

The prefrontal cortex and its interactions with the amygdala and ventral striatum

In the rat, the PFC is a heterogeneous region of the brain that includes the prelimbic, anterior cingulate, agranular insular and orbitofrontal areas [164], [269]. Each of these regions makes a distinct contribution to emotional or motivational influences on behaviour. Though the contribution of the PFC to conditioning is likely complex, and certainly not understood in detail, recent studies have shed some light on the processes that might be subserved by prefrontal cortical subregions, and on

Conclusions

Emotion, motivation and reinforcement are not unitary. Pavlovian conditioning creates multiple representations (Fig. 1), whose neural bases are dissociable and gradually becoming clear. These include CS–US(sensory) or S–S associations, dependent at least in part on the perirhinal cortex for visual stimuli and on the gustatory neocortex for food USs; CS–US(motivational) associations, suggested to depend on the BLA for both appetitive and aversive conditioning; direct CS–affect associations,

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