Valence coding in amygdala circuits
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.
References (108)
- et al.
A framework for studying emotions across species
Cell
(2014) - et al.
Re-valuing the amygdala
Curr Opin Neurobiol
(2010) - et al.
Decoding the nature of emotion in the brain
Trends Cogn Sci
(2016) Understanding emotion with brain networks
Curr Opin Behav Sci
(2018)Divergent routing of positive and negative information from the amygdala during memory retrieval
Neuron
(2016)- et al.
Searching for learning-dependent changes in the antennal lobe: simultaneous recording of neural activity and aversive olfactory learning in honeybees
Front Behav Neurosci
(2010) Neuronal representation of social information in the medial amygdala of awake behaving mice
Cell
(2017)- et al.
The primate amygdala represents the positive and negative value of visual stimuli during learning
Nature
(2006) - et al.
Basolateral amygdala circuitry in positive and negative valence
Curr Opin Neurobiol
(2018) - et al.
Amygdala microcircuits controlling learned fear
Neuron
(2014)
Optogenetic activation of the central amygdala generates addiction-like preference for reward
Eur J Neurosci
Integrated control of predatory hunting by the central nucleus of the amygdala
Cell
A circuit mechanism for differentiating positive and negative associations
Nature
Amygdala interneuron subtypes control fear learning through disinhibition
Nature
Neuronal oscillations in cortical networks
Science
4-Hz oscillations synchronize prefrontal-amygdala circuits during fear behavior
Nat Neurosci
The fear circuit of the mouse forebrain: connections between the mediodorsal thalamus, frontal cortices and basolateral amygdala
Eur J Neurosci
Estrogen receptor-α in medial amygdala neurons regulates body weight
J Clin Invest
Loss of intercalated cells (ITCs) in the mouse amygdala of Tshz1 mutants correlates with fear, depression, and social interaction phenotypes
J Neurosci
A central amygdala-substantia innominata neural circuitry encodes aversive reinforcement signals
Cell Rep
Distinct roles for direct and indirect pathway striatal neurons in reinforcement
Nat Neurosci
Selective erasure of a fear memory
Science
Synapse-specific astrocyte gating of amygdala-related behavior
Nat Neurosci
Differential recruitment of competing valence-related amygdala networks during anxiety
Neuron
Diverging neural pathways assemble a behavioural state from separable features in anxiety
Nature
Bidirectional switch of the valence associated with a hippocampal contextual memory engram
Nature
The Conceptual Representation and the Measurement of Psychological Forces
A circumplex model of affect
J Pers Soc Psychol
The Study of Instinct
Novelty-suppressed feeding in the mouse
The Organization of Behavior: A Neuropsychological Theory
Echoes of affective stimulation in brain connectivity networks
Cereb Cortex
Functional circuits and anatomical distribution of response properties in the primate amygdala
J Neurosci
Two parallel pathways assign opposing odor valences during Drosophila memory formation
Cell Rep
An anatomical investigation of the temporal lobe in the monkey (Macaca mulatta)
J Comp Neurol
From circuits to behaviour in the amygdala
Nature
Behavioral changes associated with ablation of the amygdaloid complex in monkeys
J Comp Physiol Psychol
The amygdaloid complex: anatomy and physiology
Physiol Rev
What is the amygdala?
Trends Neurosci
Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning
J Neurosci
Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal
Proc Natl Acad Sci U S A
Architectural representation of valence in the limbic system
Neuropsychopharmacology
Organization of valence-encoding and projection-defined neurons in the basolateral amygdala
Cell Rep
Multi-dimensional coding by basolateral amygdala neurons
Neuron
Basolateral to central amygdala neural circuits for appetitive behaviors
Neuron
Optogenetic excitation of central amygdala amplifies and narrows incentive motivation to pursue one reward above another
J Neurosci
Encoding of conditioned fear in central amygdala inhibitory circuits
Nature
Central amygdala circuits modulate food consumption through a positive-valence mechanism
Nature Neurosci
Quantified coexpression analysis of central amygdala subpopulations
eNeuro
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Nature
Cited by (45)
The effect of emotional faces on reward-related probability learning in depressed patients
2024, Journal of Affective DisordersPerineuronal net structure as a non-cellular mechanism contributing to affective state: A scoping review
2024, Neuroscience and Biobehavioral Reviews