Cortical oscillations arise from contextual interactions that regulate sparse coding

Significance The nature and functions of oscillations in cerebral cortex are complex and controversial, and the mechanisms that regulate them are poorly understood. We propose a regulatory mechanism that links the dynamical state of the cortex to interactions between sensory and behavioral context during information processing. We explain how a prominent set of otherwise paradoxical empirical results can be understood with a single free parameter, the ratio of monosynaptic to disynaptic input to a subpopulation of inhibitory cells. In particular, we show that the power and frequency of gamma-range oscillations can be used to monitor the state of a cortical network. Our proposed model makes specific predictions that have broad implications for the basic understanding of information coding in the cortex. Precise spike times carry information and are important for synaptic plasticity. Synchronizing oscillations such as gamma bursts could coordinate spike times, thus regulating information transmission in the cortex. Oscillations are driven by inhibitory neurons and are modulated by sensory stimuli and behavioral states. How their power and frequency are regulated is an open question. Using a model cortical circuit, we propose a regulatory mechanism that depends on the activity balance of monosynaptic and disynaptic pathways to inhibitory neurons: Monosynaptic input causes more powerful oscillations whereas disynaptic input increases the frequency of oscillations. The balance of stimulation to the two pathways modulates the overall distribution of spikes, with stronger disynaptic stimulation (e.g., preferred stimuli inside visual receptive fields) producing high firing rates and weak oscillations; in contrast, stronger monosynaptic stimulation (e.g., suppressive contextual stimulation from outside visual receptive fields) generates low firing rates and strong oscillatory regulation of spike timing, as observed in alert cortex processing complex natural stimuli. By accounting for otherwise paradoxical experimental findings, our results demonstrate how the frequency and power of oscillations, and hence spike times, can be modulated by both sensory input and behavioral context, with powerful oscillations signifying a cortical state under inhibitory control in which spikes are sparse and spike timing is precise.