Basolateral amygdala circuitry in positive and negative valence

Abstract

All organisms must solve the same fundamental problem: they must acquire rewards and avoid danger in order to survive. A key challenge for the nervous system is therefore to connect motivationally salient sensory stimuli to neural circuits that engage appropriate valence-specific behavioral responses. Anatomical, behavioral, and electrophysiological data have long suggested that the amygdala plays a central role in this process. Here we review experimental efforts leveraging recent technological advances to provide previously unattainable insights into the functional, anatomical, and genetic identity of neural populations within the amygdala that connect sensory stimuli to valence-specific behavioral responses.

Figure 1. Positive and negative value-coding neurons in the amygdala

A. Response profiles of two representative value-coding neurons in the primate amygdala recorded during a reversal learning task. A positive value-coding neuron (left) increases its firing rate to a CS that predicts an appetitive US (blue lines) while a negative value-coding neuron (right) responds to a CS that predicts an aversive US (red lines). Note that these neurons reflect the value of a CS rather than its identity, as they maintain value-coding after reinforcement contingencies are switched (solid lines, pre-reversal, dashed lines, postreversal). For details, see [44]. B. CS and US response profiles in a population of positive value-coding (left) or negative value-coding (right) neurons across 20 trials following a reversal in reinforcement contingencies. The color code plots the average normalized difference in activity on rewarding and aversive trials where a z-score of 0 means there is no difference in response to an appetitive vs aversive CS. Immediately after reversal (trial 1), there is discordance between CS and US selectivity (different colors after CS and US appearance on trial 1 for both populations). With learning, CS responses, at the population level, come to match US responses (same color after CS and US). For details, see [29]. Reproduced with permission from [29] and [44].

Figure 2. Anatomical connectivity and genetic identity of positive and negative value-coding BLA neurons

A model, based on the integration of findings from [48, 52, 70, 74], in which genetic markers and anatomical connections from the BLA to the nucleus accumbens and central amygdala determine valence-specific behaviors. Green = neurons activated by rewarding stimuli. Red = neurons activated by aversive stimuli. Solid line = excitatory connection. Dashed line = inhibitory connection. Ppp1rlb = protein phosphatase 1 regulatory inhibitor subunit 1B. Rspo2 = R-spondin 2. Sst = somatostatin. Nts = neurotensin. Tac2 = tachykinin 2. *Note that the activity of somatostatin-expressing neurons in the central amygdala has also been shown to be able to elicit defensive behaviors [75].