Control of innate olfactory valence by segregated cortical amygdala circuits.

Autor:	Howe JR; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA.; Neurosciences Graduate Program, University of California, San Diego, La Jolla, CA 92093, USA.; Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA.; These authors contributed equally., Chan CL; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA.; These authors contributed equally., Lee D; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA., Blanquart M; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA., Lee JH; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA., Romero HK; Neurosciences Graduate Program, University of California, San Diego, La Jolla, CA 92093, USA.; Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA.; Center for Circadian Biology, University of California, San Diego, La Jolla, CA 92093, USA., Zadina AN; Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, 10027, USA., Lemieux ME; Salk Institute for Biological Sciences, La Jolla, CA 92037, USA., Mills F; Salk Institute for Biological Sciences, La Jolla, CA 92037, USA., Desplats PA; Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA.; Center for Circadian Biology, University of California, San Diego, La Jolla, CA 92093, USA.; Department of Pathology, University of California, San Diego, La Jolla, CA 92093, USA., Tye KM; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA.; Salk Institute for Biological Sciences, La Jolla, CA 92037, USA.; Howard Hughes Medical Institute, La Jolla, CA 92037, USA., Root CM; Department of Neurobiology, University of California, San Diego, La Jolla, CA 92093, USA.
Jazyk:	angličtina
Zdroj:	BioRxiv : the preprint server for biology [bioRxiv] 2024 Oct 22. Date of Electronic Publication: 2024 Oct 22.
DOI:	10.1101/2024.06.26.600895
Abstrakt:	Animals exhibit innate behaviors that are stereotyped responses to specific evolutionarily relevant stimuli in the absence of prior learning or experience. These behaviors can be reduced to an axis of valence, whereby specific odors evoke approach or avoidance responses. The posterolateral cortical amygdala (plCoA) mediates innate attraction and aversion to odor. However, little is known about how this brain area gives rise to behaviors of opposing motivational valence. Here, we sought to define the circuit features of plCoA that give rise to innate attraction and aversion to odor. We characterized the physiology, gene expression, and projections of this structure, identifying a divergent, topographic organization that selectively controls innate attraction and avoidance to odor. 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 attraction and avoidance, 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 cell types, whereby anterior glutamatergic neurons preferentially express VGluT2 and posterior neurons express VGluT1 . Activation of these respective cell types recapitulates appetitive and aversive behaviors, and chemogenetic inhibition reveals partial necessity for responses to innate appetitive or aversive odors. Finally, we identified topographically organized circuits defined by 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 advance our understanding of how the olfactory system generates stereotypic, hardwired attraction and avoidance, and supports 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. This suggests a novel amygdala circuit motif in which valence encoding is represented not by the firing properties of individual neurons, but by population level identity encoding that is routed through divergent targets to mediate distinct behaviors of opposing appetitive and aversive responses. Competing Interests: DECLARATION OF INTERESTS The authors declare no competing interests.
Databáze:	MEDLINE
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