A Novel Olfactory Circuit Promotes Social Learning

Abstract

To acquire resources and avoid predation, wild animals must be capable of fast learning. One form of fast learning, the Social Transmission of Food Preferences (STFP), enables mice to trust unfamiliar food odors after smelling them on the breath of conspecifics. STFP is known to involve a sparse population of guanylate cyclase D (GCD)-expressing olfactory sensory neurons, as well as the cholinergic basal forebrain and various classic centers of learning and memory. It is not known how these disparate brain regions are recruited during the acquisition of social food preferences. Here, we describe a novel population of olfactory bulb projection neurons (GCD-PNs) that sample from GCD glomeruli in the bulb and project to both canonical bulb targets as well as the vertical limb of the nucleus of the diagonal band of Broca (vNDB). Through rabies tracing and fiber photometry we demonstrate that GCD-PNs interface with a variety of genetically defined populations in the vNDB, including cholinergic neurons. We further find GCD-PN axons in the vNDB to be both necessary and sufficient for the formation of social food preferences. Finally, we demonstrate that GCD-PN activity drives a variety of behavioral changes outside the context of STFP. The discovery of functional GCD-PN axons in the vNDB represents one of the shortest known links between primary sensation and cholinergic neuromodulation, and suggests a novel mechanism for bottom-up recruitment of acetylcholine in situations that require immediate learning.