Nonlinear cross-frequency interactions in primary auditory cortex spectrotemporal receptive fields: a Wiener-Volterra analysis

The effects of nonlinear interactions between different sound frequencies on the responses of neurons in primary auditory cortex (AI) have only been investigated using two-tone paradigms. Here we stimulated with relatively dense, Poisson-distributed trains of tone pips (with frequency ranges spanning five octaves, 16 frequencies /octave, and mean rates of 20 or 120 pips /s), and examined within-frequency (or auto-frequency) and cross-frequency interactions in three types of AI unit responses by computing second-order "Poisson-Wiener" auto- and cross-kernels. Units were classified on the basis of their spectrotemporal receptive fields (STRFs) as "double-peaked", "single-peaked" or "peak-valley". Second-order interactions were investigated between the two bands of excitatory frequencies on double-peaked STRFs, between an excitatory band and various non-excitatory bands on single-peaked STRFs, and between an excitatory band and an inhibitory sideband on peak-valley STRFs. We found that auto-frequency interactions (i.e., those within a single excitatory band) were always characterized by a strong depression of (first-order) excitation that decayed with the interstimulus lag up to similar to 200 ms. That depression was weaker in cross-frequency compared to auto-frequency interactions for similar to 25% of dual-peaked STRFs, evidence of "combination sensitivity" for the two bands. Non-excitatory and inhibitory frequencies (on single-peaked and peak-valley STRFs, respectively) typically weakly depressed the excitatory response at short interstimulus lags (< 50 ms), but weakly facilitated it at longer lags (similar to 50-200 ms). Both the depression and especially the facilitation were stronger for interactions with inhibitory frequencies rather than just non-excitatory ones. Finally, facilitation in single-peaked and peak-valley units decreased with increasing stimulus density. Our results indicate that the strong combination sensitivity and cross-frequency facilitation suggested by previous two-tone-paradigm studies are much less pronounced when using more temporally-dense stimuli.