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 4 from where activity propagates to associative layer 2/3. It is currently not known whether there is a particular organization of neuronal population activity that is stable across layers and sound levels during sound processing. 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 neural 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. Thus, spontaneous and evoked activity in both L4 and L2/3 of A1 are composed of neuronal avalanches with similar power law relationships. Our results demonstrate network principles linked to maximal dynamic range, optimal information transfer and matching complexity between L4 and L2/3 to shape population activity in auditory cortex.