Abstract
Corticofugal projections to evolutionarily ancient, subcortical 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, supralinear excitatory postsynaptic potential summation, indicating that descending signals can nonlinearly 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.
Highlights
IntroductionThe auditory system is organized as a network of feedback loops, such that most central auditory nuclei receive descending projections from higher levels of the processing hierarchy (Diamond et al, 1969; Saldaña et al, 1996; Winer et al, 1998; Winer et al, 2001; Doucet et al, 2003; Coomes and Schofield, 2004; Schofield et al, 2006; Suthakar and Ryugo, 2017)
Corticofugal axons are predominantly restricted to the shell inferior colliculus (IC), but little is known about the extent of functional synaptic connectivity between auditory cortex and IC neurons
Single flashes of blue light from an optic fiber positioned over auditory cortex (1–5 ms duration) reliably triggered excitatory postsynaptic potentials (EPSPs) in n = 21/38 IC neurons recorded from N = 8 mice (Figure 1B)
Summary
The auditory system is organized as a network of feedback loops, such that most central auditory nuclei receive descending projections from higher levels of the processing hierarchy (Diamond et al, 1969; Saldaña et al, 1996; Winer et al, 1998; Winer et al, 2001; Doucet et al, 2003; Coomes and Schofield, 2004; Schofield et al, 2006; Suthakar and Ryugo, 2017). The auditory cortex is a major source of excitatory (glutamatergic) descending projections, with the density of descending fibers often rivaling that of ascending fiber tracts (Winer et al, 2001; Winer, 2006; Stebbings et al, 2014). These corticofugal projections likely play a major role in hearing by providing an anatomical substrate for ‘top-d own’ information to control early acoustic processing. Stimulating or silencing the auditory cortex in vivo changes spontaneous and sound-evoked activity throughout the Oberle et al eLife 2021;10:e72730.
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