Multidimensional processing in the amygdala

Abstract

Brain-wide circuits that coordinate affective and social behaviours intersect in the amygdala. Consequently, amygdala lesions cause a heterogeneous array of social and non-social deficits. Social behaviours are not localized to subdivisions of the amygdala even though the inputs and outputs that carry social signals are anatomically restricted to distinct subnuclear regions. This observation may be explained by the multidimensional response properties of the component neurons. Indeed, the multitudes of circuits that converge in the amygdala enlist the same subset of neurons into different ensembles that combine social and non-social elements into high-dimensional representations. These representations may enable flexible, context-dependent social decisions. As such, multidimensional processing may operate in parallel with subcircuits of genetically identical neurons that serve specialized and functionally dissociable functions. When combined, the activity of specialized circuits may grant specificity to social behaviours, whereas multidimensional processing facilitates the flexibility and nuance needed for complex social behaviour.

Fig. 1 |. Alternative functional organization schemes of the primate amygdala.

a | One view of primate amygdala organization is that specialized neurons, which are narrowly tuned to a single stimulus or task parameter, form clusters that follow, to some extent, the anatomical target or origin of inputs and outputs, respectively. b | An alternative view of primate amygdala organization is that multidimensional neurons are distributed quasi-equally across the nuclei of the amygdala. As indicated in the key, the colours represent a subset of the known stimulus categories that activate the amygdala^,,, with the exception of visceral inputs, for which there is limited evidence. The proportion of neurons that respond to each type of input is unknown. AB, accessory basal nucleus; B, basal nucleus; CeA, central nucleus of the amygdala; L, lateral nucleus; Me, medial nucleus.

Fig. 2 |. Face-responsive neurons show non-linear combinations of selectivity.

a–d | This neuron was recorded from the basal nucleus of the amygdala in response to the passive viewing of face images that represented specific combinations of identity and facial expression. The stimuli in each row of images depict three facial expressions displayed by the same individual. The three columns correspond to appeasing (lip-smack), neutral and aggressive (threat) facial expressions. Rasters (top) and peri-event time histograms (bottom) are shown below each stimulus face and their analysis indicates that this neuron responded to the appeasing facial expression of the monkeys in parts a and b and to the threatening expressions of the monkeys in parts c and d. Analysis of variance showed that there was a significant interaction (P < 0.001) between identity and facial expression. Parts a–d reprinted with permission from REF., American Physiological Society.

Fig. 3 |. Multidimensional selectivity arises from the intersection of brain-wide circuits.

The amygdala (represented here by the circle in the centre of the image) receives inputs from, and sends outputs to, numerous brain areas, giving rise to a complex web of intranuclear and internuclear connections (as indicated by the coloured lines) and closing circuits that carry out quasi-dissociable functions. The six main functions represented in the ring around the central circle were chosen because they are obligatory components of social behaviours; a truncated list of the brain areas that are connected to the amygdala and involved in the specified function is given in each box. The list of connected areas is by no means complete and does not reflect the level of detail gained from anatomical studies. The multicoloured circles represent multidimensional neurons in the amygdala; each colour represents a stimulus from the brain areas highlighted in the same colour.