Auditory corticofugal neurons transmit non-auditory signals to support discriminative learning

Abstract

Layer 5 pyramidal neurons of sensory cortices project "corticofugal" axons to myriad sub-cortical targets, thereby broadcasting high-level signals important for perception and learning. Recent studies suggest dendritic Ca2+ spikes as key biophysical mechanisms supporting corticofugal neuron function: These long-lasting events drive burst firing, thereby initiating uniquely powerful signals to modulate sub-cortical representations and trigger learning-related plasticity. However, the behavioral relevance of corticofugal dendritic spikes is poorly understood. We shed light on this issue using 2-photon Ca2+ imaging of auditory corticofugal dendrites as mice of either sex engage in a GO/NO-GO sound-discrimination task. Unexpectedly, only a minority of dendritic spikes were triggered by behaviorally relevant sounds under our conditions. Task related dendritic activity instead mostly followed sound cue termination and co-occurred with mices instrumental licking during the answer period of behavioral trials, irrespective of reward consumption. Temporally selective, optogenetic silencing of corticofugal neurons during the trial answer period impaired auditory discrimination learning. Thus, auditory corticofugal systems contribution to learning and plasticity may be partially non-sensory in nature. Significance StatementThe auditory cortex sends a massive "feedback" projection to the inferior colliculus (IC) which controls IC neuron plasticity and some types of perceptual learning. Precisely what signals are fed back during behavior is unclear. Using multiphoton imaging of auditory cortico-collicular neurons as mice engage in a sound discrimination task, we find that activity coincides more with mices instrumental actions rather than sound cues. Dendritic Ca2+ spikes and burst firing contributed to this non-auditory activity, which is notable given that dendritic spikes instruct synaptic plasticity in many other circuits. Accordingly, optogenetic silencing of corticofugal neurons during mices instrumental actions impaired discriminative learning. Auditory corticofugal neurons may thus transmit significant non-auditory information that contributes to learning-related plasticity.