Presentation Details
A Sensory Circuit for Social Learning

Kara A.Fulton1, Slater Sharp1, Gloria DuMaine1, Sidharth Annapragada1, Phelipe E.Silva1, 2, Sebastian Kruettner1, 3, Emma Robinson1, 4, Sandeep R.Datta1.

1Harvard Medical School, Boston, MA, USA.2University of São Paulo, São Paulo, Brazil.3Broad Institute, Cambridge, MA, USA.4Scripps Research Institute, La Jolla, CA, USA

Abstract


In social contexts, mice can learn about the safety of food through an association formed between food odors and the semiochemicals present in the breath or feces of other mice. This behavior is known as the social transmission of food preference and is mediated through the necklace olfactory subsystem via the Guanylyl Cyclase D (GCD) olfactory receptors (Munger et al., 2010). However, it remains unclear how the sensory information encoded by the GCD neurons are transmitted to the rest of the brain and how the olfactory system supports this form of social learning. Through a combination of viral tracing and optogenetics, we have identified a circuit between the GCD projection neurons in the olfactory bulb and basal forebrain which is necessary and sufficient for this olfactory-mediated social learning. The connectivity of the GCD olfactory circuit with the basal forebrain suggests that this network is suited not only for processing social odors, but also for improving learning. Indeed, activation of GCD projection neurons (through odor ligands, optogenetics, or chemogenetics) activates neurons in the basal forebrain and evokes acetylcholine release as measured through fiber photometry or GRIN-based calcium imaging. Collectively, our data suggests that the necklace olfactory system is functionally connected to the cholinergic system that is important for learning and memory. In addition to promoting social learning of food preferences, chemogenetic or optogenetic activation of GCD neurons enhances memory formation during social recognition and novel object tasks and enables optimal spatial navigation in complex environments. We propose that this sensory circuit may have evolved to recruit attention to support learning in a variety of ethological conditions which require flexible behavior. 

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