The Descending Subnetwork Of Layer 5 Of Auditory Cortex Independently Governs Innate And Learned Behaviors

Animals rely on both innate and learned behaviors to survive in their natural environment.These behaviors are triggered by external sensory stimuli,with auditory stimuli being particularly important.The auditory cortex,which serves as the central hub for processing auditory information,plays a critical role in the two types of behavioral responses to sound.Previous studies have shown that the AC-TS loop is involved in learned auditory discrimination behavior,while the AC-IC loop is responsible for encoding innate defense behavior induced by sound.Most of the descending projections in the auditory cortex are carried out by pyramidal neurons located in layer 5.These projection neurons distribute information to various cortical and subcortical structures by sending axonal projections to different targets.Since the output from layer 5 neurons is currently the only known substrate that can directly affect behavior in the cortex,it remains to be determined whether these projection neurons encode innate and learned behaviors independently by participating in different projection loops in parallel.In this study,we examined whether a subset of layer 5 pyramidal neuron projections in the auditory cortex encode different types of behavioral information independently.To achieve this,we designed a learned auditory discrimination task involving the auditory cortex and auditory striatum,and an innate sound-induced flight behavior involving the auditory cortex and inferior colliculus projection.By using chemogenetic and optogenetic manipulation of a subset of layer 5 pyramidal neurons,we discovered that TS projection neurons are primarily responsible for learned discrimination behaviors,whereas IC projection neurons are crucial for innate defense behaviors.We also found that there is an asymmetric microloop structure with dense connections within the same neuronal population and few connections between different subpopulations.Additionally,IC projection neurons show lower thresholds and wider frequency tuning than TS projection neurons.Our results suggest that TS projection neurons and IC projection neurons form physically dispersed and functionally separated subnetworks that can independently transmit auditory information to downstream targets and control innate and learned behaviors in parallel.These findings shed light on the ability of the cortex,as the central hub for sensory information,to regulate specific brain regions to accurately code behavior,rather than merely broadcasting to multiple nuclei.