Valence coding in amygdala circuits

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Highlights

  • Populations of the amygdala complex drive positive and negative valence.

  • Valence coding can be defined by neural responses to positive and negative stimuli.

  • Recordings of photoidentified populations revealed valence coding biases.

  • CeA populations have mainly been defined by gene markers.

  • BLA populations have mainly been defined by their projections targets.

The neural mechanisms underlying emotional valence are at the interface between perception and action, integrating inputs from the external environment with past experiences to guide the behavior of an organism. Depending on the positive or negative valence assigned to an environmental stimulus, the organism will approach or avoid the source of the stimulus. Multiple convergent studies have demonstrated that the amygdala complex is a critical node of the circuits assigning valence. Here we examine the current progress in identifying valence coding properties of neural populations in different nuclei of the amygdala, based on their activity, connectivity, and gene expression profile.

Section snippets

The concept of valence

Across the animal kingdom, environmental stimuli can elicit a repertoire of behavioral responses ranging from approach to avoidance. Valence is the subjective value assigned to sensory stimuli which determines subsequent behavior. Positive valence leads to approach and consummatory behaviors while negative valence leads to defensive and avoidance behaviors [1,2]. For many sensory stimuli the assigned valence is innate, however, valence is weighted by the internal state of the organism and by

Valence coding in populations of the central amygdala (CeA)

The CeA is the main output of the amygdala and has primarily been studied in the context of fear-related behaviors [28]. However, the CeA has also repeatedly been reported to promote appetitive behaviors [29••,30,31]. Although contradictory, these results could be supported by divergent activity of distinct neural populations. Extensive research has been dedicated to identify the function of gene-defined and projection-defined populations within the capsular, lateral, and medial areas of the

Valence coding in populations of the basolateral amygdala (BLA)

Multiple studies have performed single-unit recordings in the BLA during stimuli of both positive and negative valence. Although direct optogenetic stimulation of the lateral amygdala (LA) can elicit a defensive response in a naïve mouse [51], recordings of BLA neurons in monkeys, rats and mice have shown that around 50% of the units respond to predictive cues of positive or negative valence [12••,21,27], with an overrepresentation of neurons responding to positive valence in monkeys [21] and

Valence in other amygdala nuclei

Most studies analyze the origin of valence in the CeA and BLA but surrounding amygdaloid nuclei also regulate valence. For example, direct optogenetic activation of the basomedial amygdala (BMA, Figure 1) is anxiogenic, as the optogenetic activation of the vmPFC inputs to this nucleus [70]. Interestingly, the BMA directly projects to the ventromedial hypothalamus (VMH) which regulates defensive and social behaviors [71].

Neurons in the medial amygdala (MeA, Figure 1) have repeatedly been shown

Moving forward to crack the valence code

Gain and loss of function experiments have demonstrated that neuronal subpopulations of the amygdala defined by their projection targets or gene expression can drive behaviors of opposite valence (Figure 3). Activity-dependent markers and electrophysiological recordings have revealed that average activity of a population is generally consistent with the driven behaviors (Figure 3c). Yet, recordings revealing single-unit heterogeneity in valence coding within populations [12••,53] suggest the

Conclusions

Over the last decade, the study of valence coding in the amygdala has made unprecedented progress by revealing elaborate genetic and anatomical circuits differentially involved in positive and negative valence (Figure 3). This exceptional leap forward is the fruit of technological advancements combined with the spread of systematic behavioral testing of both positive and negative valence in the same experiment. Beyond this experimental prerequisite, recent studies have even started to combine

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Joanna Dabrowska, Mario Martin-Fernandez, Sebastien Delcasso, Xavier Leinekugel, Gwendolyn Calhoon, Caitlin Vander Weele and Praneeth Namburi for critical reading of the manuscript. We acknowledge support by the Région Nouvelle-Aquitaine and INSERM-Avenir to the Beyeler Lab and by the Brain and Behavior Research Foundation NARSAD young investigator grant to AB.

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