Recurrent Circuits Amplify Corticofugal Signals and Drive Feedforward Inhibition in the Inferior Colliculus

• DOI: 10.1523/jneurosci.0626-23.2023
• Publication Date: 2023-06-12T17:50:14Z
• Authors: Hannah M. Oberle; Alexander N. Ford; Jordyn E. Czarny; Meike M. Rogalla; Pierre F. Apostol...
• Keywords: Superior olivary complex

The inferior colliculus (IC) is a midbrain hub critical for perceiving complex sounds, such as speech. In addition to processing ascending inputs from most auditory brainstem nuclei, the IC receives descending cortex that control neuron feature selectivity, plasticity, and certain forms of perceptual learning. Although corticofugal synapses primarily release excitatory transmitter glutamate, many physiology studies show cortical activity has net inhibitory effect on spiking. Perplexingly, anatomy imply axons target glutamatergic neurons while only sparsely innervating GABA neurons. Corticofugal inhibition may thus occur largely independently feedforward activation local We shed light this paradox using in vitro electrophysiology acute slices fluorescent reporter mice either sex. Using optogenetic stimulation axons, we find excitation evoked with single flashes indeed stronger presumptive compared GABAergic However, fire tonically at rest, sparse weak suffices significantly increase their spike rates. Furthermore, subset spikes during repetitive activity, leading polysynaptic owing dense intracollicular connectivity. Consequently, recurrent amplifies drives neurons, generates substantial IC. Thus, signals engage circuits despite apparent constraints monosynaptic connectivity between SIGNIFICANCE STATEMENT Descending “corticofugal” projections are ubiquitous across mammalian sensory systems, enable neocortex subcortical predictive or feedback manner. glutamatergic, neocortical often inhibits How does an pathway generate inhibition? Here study (IC), important sound perception. Surprisingly, cortico-collicular transmission was onto triggered glutamate thereby generating strong spiking Our results reveal novel mechanism recruits limited convergence networks.