Control of innate olfactory valence by segregated cortical amygdala circuits

Abstract

Animals exhibit innate behaviors that are stereotyped responses to specific evolutionarily relevant stimuli in the absence of prior learning or experience. The posterolateral cortical amygdala (plCoA) mediates innate attraction and aversion to odor. Here, we sought to define the circuit features of plCoA that give rise to innate attraction and aversion to odor in mice. First, we examined odor-evoked responses in these areas and found sparse encoding of odor identity, but not valence. We next considered a topographic organization and found that optogenetic stimulation of the anterior and posterior domains of plCoA elicits avoidance and attraction, respectively, suggesting a functional axis for valence. Using single-cell and spatial RNA sequencing, we identified the molecular cell types in plCoA, revealing an anteroposterior gradient in glutamatergic neurons that are sufficient and partially necessary for behavior. Finally, we identified topographically organized projections, whereby anterior neurons preferentially project to medial amygdala, and posterior neurons preferentially project to nucleus accumbens, which are respectively sufficient and necessary for innate attraction and aversion. Together, these data support a model whereby distinct, topographically distributed plCoA populations direct innate olfactory responses by signaling to divergent valence-specific targets, linking upstream olfactory identity to downstream valence behaviors, through a population code.

Keywords: cortical amygdala; innate behavior; mouse; neuroscience; odor; topographic organization; valence.