Re-valuing the amygdala

Abstract

Recent advances indicate that the amygdala represents valence: a general appetitive/aversive affective characteristic that bears similarity to the neuroeconomic concept of value. Neurophysiological studies show that individual amygdala neurons respond differentially to a range of stimuli with positive or negative affective significance. Meanwhile, increasingly specific lesion/inactivation studies reveal that the amygdala is necessary for processes--for example, fear extinction and reinforcer devaluation--that involve updating representations of value. Furthermore, recent neuroimaging studies suggest that the human amygdala mediates performance on many reward-based decision-making tasks. The encoding of affective significance by the amygdala might be best described as a representation of state value-a representation that is useful for coordinating physiological, behavioral, and cognitive responses in an affective/emotional context.

Figure 1

Individual neurons in primate amygdala can encode positive or negative visual stimulus value. (a) Sequence of events during an appetitive/aversive trace conditioning task; for details, see [26]. In each session, the subject learns to associate three novel, abstract visual stimuli with large reward, small reward, or an aversive air-puff to the face. After the initial reward contingencies are learned, a reversal takes place: the image associated with large reward is now followed by air-puff, and the image associated with air-puff is now followed by large reward. The reversal allows neural signals related to image value to be disentangled from neural signals related to visual characteristics of the images. (b and c) Examples of amygdala neurons that encode image value during the task shown in a. Plots are peri-stimulus time histograms aligned on the time of image presentation (black dotted line). Blue line, activity during large reward trials. Cyan line, activity during small reward trials. Red line, activity during air-puff trials. (b) A positive value-coding neuron, which fires more strongly on large reward trials than air-puff trials. (c) A negative value-coding neuron, which fires more strongly on air-puff trials than on large-reward-trials. Note that the activity on small reward trials is intermediate; for details, see [27•]. Differential activity may occur primarily during image presentation (as in c), the trace interval (as in b), or both.

Figure 2

Populations of neurons in primate amygdala encode the value of conditioned stimuli, of unconditioned stimuli and of a fixation point. (a and b) Population responses to conditioned and unconditioned stimuli in a trace conditioning task in which novel, abstract images are followed by either reward or air-puff. Plots are normalized and averaged peri-stimulus time histograms (PSTHs) aligned on the time of CS presentation (vertical dashed line). Reward or air-puff occurred at either 1.8 or 1.85 s, depending on the session. Blue line, activity on rewarded trials. Red line, activity on air-puff trials. Shading indicates SEM. Inset histograms, reinforcement selectivity indices calculated for each neuron using an ROC analysis; see [29•] for details. (a) Population responses of positive value-coding cells. Note that US selectivity indices are predominantly greater than 0.5, indicating a higher firing rate for reward than for air-puff. (b) Population responses of negative value-coding cells. Note that US selectivity indices are predominantly less than 0.5, indicating a higher firing rate for air-puff than for reward. (c) Population normalized average response to fixation point (FP) presentation for positive value-coding cells (blue), negative value-coding cells (red), and non-value-coding cells (black). Shaded areas indicate SEM. Note that the FP is a mildly positive stimulus, and that positive and negative value-coding cells respond to it in a manner consistent with their responses to CSs; see [27•] for details. (d) Bar chart showing the percentage of cells with increases (blue), decreases (red), or no change (black) in activity during FP presentation. The number of cells of each type is indicated. The majority of positive value-coding cells increase firing to the FP, while the majority of negative value-coding cells decrease firing to the FP. Figure adapted with permission from [27•] and [29•].

Figure 3

Neurons in the rat BLA develop preferential responses to a rewarded cue. (a and b) Responses of a BLA neuron in the discriminative stimulus (DS) task, in which rats learned to press a lever in response to an auditory cue (the DS) to receive sucrose. Another interleaved auditory cue, the nonrewarded stimulus (NS), was not reinforced. (a) Response of an example BLA neuron to the DS. (b) Response of the same neuron to the NS. Rasters and peri-stimulus time histograms are aligned on cue presentation. (c and d) Population average normalized firing rate of nucleus accumbens core (NAc) neurons to the DS before and after injection of a vehicle (c) or baclofen and muscimol (B/M) (d) into the bilateral BLA. Shading indicates SEM. Inactivation of BLA dramatically reduced the discrimination of the DS and NS by NAc neurons; for further details, see [40•]. Figure adapted with permission from [40•].

Figure 4

Schematic diagram of a reinforcer devaluation task. In the training phase, the subject learns to associate pairs of cues with one of two food reward (e.g., peanuts and raisins) or non-reinforcement. Typically a large set of cue pairs is used, although only two are shown here. After training, and before testing, the subject is offered free access to one of the rewards (e.g., peanuts) until satiation (the subject voluntarily stops consumption of the reward). The monkey’s reward preferences are assessed both before initial training, and after satiation. In the test phase, the subject is offered a choice between cues that are associated with the devalued food (in this case, peanuts) or the non-devalued food (raisins). Normal monkeys will preferentially choose the cue associated with the non-devalued food. Monkeys lacking amygdala function continue to choose the cue associated with the devalued food; see [56] for more details.