Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus

Corticofugal projections to evolutionarily ancient, sub-cortical
structures are ubiquitous across mammalian sensory systems. These
“descending” pathways enable the neocortex to control ascending sensory
representations in a predictive or feedback manner, but the underlying
cellular mechanisms are poorly understood. Here we combine optogenetic
approaches with in vivo and in vitro patch-clamp electrophysiology to
study the projection from mouse auditory cortex to the inferior colliculus
(IC), a major descending auditory pathway that controls IC neuron feature
selectivity, plasticity and auditory perceptual learning. Although
individual auditory cortico-collicular synapses were generally weak, IC
neurons often integrated inputs from multiple corticofugal axons that
generated reliable, tonic depolarizations even during prolonged
presynaptic activity. Latency measurements in vivo showed that descending
signals reach the IC within 30 ms of sound onset, which in IC neurons
corresponded to the peak of synaptic depolarizations evoked by short
sounds. Activating ascending and descending pathways at latencies expected
in vivo caused a NMDA receptor dependent, supra-linear EPSP summation,
indicating that descending signals can non linearly amplify IC neurons’
moment-to-moment acoustic responses. Our results shed light upon the
synaptic bases of descending sensory control, and imply that
heterosynaptic cooperativity contributes to the auditory
cortico-collicular pathway’s role in plasticity and perceptual learning.