From circuits to behaviour in the amygdala

Abstract

The amygdala has long been associated with emotion and motivation, playing an essential part in processing both fearful and rewarding environmental stimuli. How can a single structure be crucial for such different functions? With recent technological advances that allow for causal investigations of specific neural circuit elements, we can now begin to map the complex anatomical connections of the amygdala onto behavioural function. Understanding how the amygdala contributes to a wide array of behaviours requires the study of distinct amygdala circuits.

Figure 1. Evolution of the amygdala across species

Primary amygdalar nuclei and basic circuit connections and function are conserved across species. An enlarged image of the basolateral complex of the amygdala (BLA) and central nucleus of the amygdala (CeA) or analogues are shown next to a coronal section from the brains of a lizard, mouse, rat, cat, monkey and human.

Figure 2. Number of studies on the amygdala

Publications on the amygdala indexed on PubMed between 1950 and 2013 demonstrate the growing interest in amygdala research.

Figure 3. Amygdalar circuits that are sufficient to alter behaviour in a diversity of domains

Projection-specific effects as shown by optogenetic or pharmacogenetic manipulation. The solid or dotted lines indicate the promotion or inhibition of certain behaviours. The basolateral complex of the amygdala (BLA) encompasses the lateral and basal nuclei. Specific cell types are shown in pink. For simplicity, projections that are anatomically or electrophysiologically defined but have not been shown to have a causal relationship with behaviour are omitted. This is a selective picture of projections that have been directly manipulated, and is not meant to signify their importance over other anatomical connections. The actual connectivity of the amygdala with other brain regions is considerably more complex. AC, auditory cortex; adBNST, anterodorsal bed nucleus of the stria terminalis; CeA, central nucleus of the amygdala; CeL, lateral CeA; CeM, medial CeA; D1R, dopamine 1 receptor; EC, entorhinal cortex; Hyp, hypothalamus; IL, infralimbic; MGN, medial geniculate nucleus; mPFC, medial prefrontal cortex; NAc, nucleus accumbens; OT, oxytocin; ovBNST, oval nucleus of the BNST; PBN, parabrachial nucleus; PKC, protein kinase C; PL, prelimbic; SOM, somatostatin; vHPC, ventral hippocampus.

Figure 4. Model of amygdala microcircuits that give rise to behaviour

New findings in the amgydala have updated our understanding of these microcircuits. Different populations of basolateral complex of the amygdala (BLA) neurons are proposed to activate distinct populations of lateral central nucleus of the amygdala (CeL) neurons to either promote fear or reduce anxiety. CeM, medial central nucleus of the amygdala; DVC, dorsal vagal complex; PAG, periaqueductal grey; PKC, protein kinase C; PVT, paraventricular nucleus of the thalamus; HYP, hypothalamus; SOM, somatostatin.

Figure 5. Interneuron and principal neuron interactions within the basolateral complex of the amygdala (BLA)

a, Model of how interneurons expressing parvalbumin (PV) and somatostatin (SOM) interact with principal neurons to mediate fear conditioning. b, The heterogeneity in PV interneuron responses is consistent with the diverse functionality of BLA principal neurons and raises the question of how BLA principal neurons may interact locally. Depicted are simplified scenarios for these interactions.