Neuronal Avalanches in Input and Associative Layers of Auditory Cortex

The primary auditory cortex processes acoustic sequences for the perception of behaviorally meaningful sounds such as speech. Sound information arrives at its input layer four from where activity propagates to associative layer 2/3. It is currently not known whether there is a characteristic organization of neuronal population activity across layers and sound levels during sound processing. Here, we identify neuronal avalanches, which in theory and experiments have been shown to maximize dynamic range and optimize information transfer within and across networks, in primary auditory cortex. We used in vivo 2-photon imaging of pyramidal neurons in cortical layers L4 and L2/3 of mouse A1 to characterize the populations of neurons that were active spontaneously, i.e., in the absence of a sound stimulus, and those recruited by single-frequency tonal stimuli at different sound levels. Single-frequency sounds recruited neurons of widely ranging frequency selectivity in both layers. We defined neuronal ensembles as neurons being active within or during successive temporal windows at the temporal resolution of our imaging. For both layers, neuronal ensembles were highly variable in size during spontaneous activity as well as during sound presentation. Ensemble sizes distributed according to power laws, the hallmark of neuronal avalanches, and were similar across sound levels. Avalanches activated by sound were composed of neurons with diverse tuning preference, yet with selectivity independent of avalanche size. Our results suggest that optimization principles identified for avalanches guide population activity in L4 and L2/3 of auditory cortex during and in-between stimulus processing.