The contribution of the amygdala, nucleus accumbens, and prefrontal cortex to emotion and motivated behaviour

Abstract

Emotion and motivation depend on the assessment of the value of environmental stimuli. Multiple representations of stimulus value are created in the brain by Pavlovian and instrumental conditioning procedures. The basolateral amygdala (BLA) appears necessary 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 (CeA) controls brainstem arousal and response systems and subserves some forms of stimulus–response Pavlovian conditioning. The nucleus accumbens (Acb) appears not to be required to represent instrumental action–outcome contingencies, but influences instrumental behaviour strongly by mediating the impact of Pavlovian CSs on instrumental responding, and is required for the normal ability of animals to choose delayed rewards. Prelimbic cortex is required for action–outcome contingency detection, while insular cortex may allow rats to remember the sensory properties of foodstuffs and thereby retrieve their specific values. The orbitofrontal cortex (OFC) may represent aspects of reinforcer value governing instrumental choice behaviour. Finally, the anterior cingulate cortex (ACC) may play a role in responding to the emotional significance of stimuli and preventing responding to inappropriate conditioned stimuli.

Introduction

Emotions and motivation both depend on our ability to assign value to events, objects, and states of the world. Such values drive our lives—thus, we seek out stimuli that are appetitive or rewarding and avoid those that are aversive. Though emotion and motivation are complex, the analysis of the neural basis of emotions has benefited from considering those brain systems that assign value to stimuli. Even within the rat there are many such systems, learning and representing different kinds of information about the world, as 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. In this review, the psychological and neural representations that govern two major classes of behaviour, Pavlovian and instrumental conditioned responding, will be summarized. Within this framework, the contributions to emotional and motivated behaviour of the amygdala, ventral striatum, and prefrontal cortex will be considered, in each case relating neural systems to the psychological representations to which they may correspond.

The term ‘Pavlovian conditioning’ (or classical conditioning) refers to a set of experimental procedures in which an experimenter arranges a contingency between stimuli in the world by presenting those stimuli independent of an animal's behaviour [1]. In a Pavlovian conditioning study, an initially neutral stimulus (such as a bell) is paired with a biologically relevant, unconditioned stimulus (US) (such as food) that normally elicits a reflexive or unconditioned response (UR) such as salivation. As a result of such pairings, the bell becomes a conditioned stimulus (CS), now capable of evoking salivation as a conditioned response (CR). Pavlovian conditioning (CS–US pairings) creates multiple associative representations in the brain [2], [3], [4], [5], [6]. Firstly, and most simply, the CS may become directly associated with the unconditioned response (UR), a stimulus–response association that carries no information about the identity of the US (e.g. Ref. [7]). However, a single US may elicit several responses; for example, a US such as a puff of air delivered to the eye may elicit a simple motor act such as blinking, and a ‘central’ process such as an enhancement of arousal or attention. Therefore, the CS may enter into stimulus–response associations with several kinds of response. Secondly, the CS can evoke a representation of affect—such as fear or the expectation of reward [8]. This embodies the concept of an emotional ‘tone’ that is tagged to a stimulus. Thirdly, the CS can become associated with the specific sensory properties of the US [4], [9], [10]—including its visual appearance, sound, feel, and smell, but also ‘consummatory’ qualities such as its taste and nutritive value.

Multiple representations are also found following instrumental conditioning, in which the experimenter arranges a contingency between the animal's behaviour and a reinforcing outcome [11]. It is apparent that at least six psychological processes contribute to learning and performance of instrumental behaviour [6], [12], [13]. Just as humans can be aware of the goals they seek, rats can conceptualize goals and actions symbolically and such representations can be in the form of declarative or semantic knowledge. Thus, goal-directed action in the rat depends on the twin representations of the instrumental contingency between an action and a particular outcome, and a representation of the outcome as a goal—termed the (instrumental) incentive value of the goal [13], [14]. Simply put, a goal-directed organism presses a lever for food because it knows (1) that lever-pressing produces food and (2) that it wants the food. What is not at all obvious intuitively is that this value, governing instrumental responding, differs from the ‘hedonic’ value that the rat experiences as it actually consumes the food. Though the instrumental incentive value normally tracks the ‘hedonic’ value closely, Dickinson and colleagues have shown in an elegant series of experiments that these values can be dissociated, being different from each other under certain circumstances [6], [12], [13]. A fourth factor governing instrumental performance is the presence of discriminative stimuli (S^Ds). When responding is rewarded in the presence of a stimulus but not in its absence, that stimulus is established as an S^D. S^Ds inform the subject that a particular instrumental (response–reinforcer) contingency is in force [15], [16], [17], though S^Ds also have properties of Pavlovian conditioned stimuli [18].

In addition to these sophisticated goal-directed systems, the rat can form stimulus–response habits, as long theorized [11], [19], [20], [21]. S–R habits are the archetype of ‘procedural’ learning: as the S–R association is direct, there is no representation of the reinforcer. If a rat is responding via a goal-directed system for food, and that food is devalued (for example, by pairing it with lithium to induce nausea), the rat will subsequently respond less for that food. However, a rat responding using its habit system, which possesses no information about the reinforcer, will not alter its rate of responding following reinforcer devaluation. Habits appear to develop with extended training; thus, overtraining can cause instrumental responses to become ‘habitual’ and resistant to reinforcer devaluation [12], [22], [23], [24], [25].

Finally, Pavlovian CSs can modulate instrumental performance [12], [13], an effect termed Pavlovian–instrumental transfer (PIT). For example, a stimulus that predicts the arrival of sucrose solution will enhance lever-pressing for sucrose [26], [27]. PIT operates both by providing general conditioned motivation [28], [29] and by selectively potentiating actions that share an outcome with the CS [18]. This Pavlovian motivational process is distinguishable from the values governing instrumental responding, psychologically (e.g. Ref. [30]) and pharmacologically [31]. PIT is functionally important as it probably plays a major role in CS-precipitated reinstatement of instrumental responding, exemplified by cue-induced relapse in drug addiction (see e.g. [32], [33], [34]).

Having summarized the psychological representations known to contribute to Pavlovian and instrumental behaviour in the rat, we will now review the contributions of the amygdala, nucleus accumbens, and prefrontal cortex to emotion and motivated behaviour, using the learning-theory framework outlined above.