Rhythmic Auditory Cortex Activity at Multiple Timescales Shapes Stimulus–Response Gain and Background Firing

Abstract

The phase of low-frequency network activity in the auditory cortex captures changes in neural excitability, entrains to the temporal structure of natural sounds, and correlates with the perceptual performance in acoustic tasks. Although these observations suggest a causal link between network rhythms and perception, it remains unknown how precisely they affect the processes by which neural populations encode sounds. We addressed this question by analyzing neural responses in the auditory cortex of anesthetized rats using stimulus-response models. These models included a parametric dependence on the phase of local field potential rhythms in both stimulus-unrelated background activity and the stimulus-response transfer function. We found that phase-dependent models better reproduced the observed responses than static models, during both stimulation with a series of natural sounds and epochs of silence. This was attributable to two factors: (1) phase-dependent variations in background firing (most prominent for delta; 1-4 Hz); and (2) modulations of response gain that rhythmically amplify and attenuate the responses at specific phases of the rhythm (prominent for frequencies between 2 and 12 Hz). These results provide a quantitative characterization of how slow auditory cortical rhythms shape sound encoding and suggest a differential contribution of network activity at different timescales. In addition, they highlight a putative mechanism that may implement the selective amplification of appropriately timed sound tokens relative to the phase of rhythmic auditory cortex activity.Key words: delta rhythm; information coding; LNP models; network state; neural coding; receptive fields IntroductionAccumulating evidence suggests that low-frequency rhythms play an important role for hearing (Schroeder and Lakatos, 2009;Giraud and Poeppel, 2012; Leong and Goswami, 2014). Neuroimaging and intracranial recordings show that neural activity in the auditory cortex (A1) at frequencies below ϳ12 Hz entrains to the temporal structure of sounds and carries information about sound identity Szymanski et al., 2011;Simon, 2012, 2013; Ng et al., 2013), possibly because natural sounds contain important acoustic structures at these frequencies Doelling et al., 2014;Gross et al., 2013). Importantly, the degree of rhythmic entrainment correlates with perceptual intelligibility (Mesgarani and Chang, 2012; Doelling et al., 2014;Peelle et al., 2013), linking the timescales relevant for acoustic comprehension with those of neural activity (Rosen, 1992;Ghitza and Greenberg, 2009; Zion Golumbic et al., 2012). Based on these results, it has been hypothesized that slow rhythmic activity in the A1 reflects key mechanisms of sound encoding that have direct consequences for hearing (Giraud and Poeppel, 2012;Peelle and Davis, 2012;Strauß et al., 2014b).This raises the central question of how precisely rhythmic auditory cortical activity shapes sensory information processing. Electrophysiological recordings showed that slow rhythms reflect fluctuatio...

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