Top-Down Influences on Local Networks: Basic Theory with Experimental Implications

The response of a population of cortical neurons to an external stimulus depends not only on the receptive field properties of the neurons, but also the level of arousal and attention or goal-oriented cognitive biases that guide information processing. These top-down effects on cortical neurons bias the output of the neurons and affect behavioral outcomes such as stimulus detection, discrimination, and response time. In any physiological study, neural dynamics are observed in a specific brain state; the background state partly determines neuronal excitability. Experimental studies in humans and animal models have also demonstrated that slow oscillations (typically in the alpha or theta bands) modulate the fast oscillations (gamma band) associated with local networks of neurons. Cross-frequency interaction is of interest as a mechanism for top-down or bottom up interactions between systems at different spatial scales. We develop a generic model of top-down influences on local networks appropriate for comparison with EEG. EEG provides excellent temporal resolution to investigate neuronal oscillations but is space-averaged on the cm scale. Thus, appropriate EEG models are developed in terms of population synaptic activity. We used the Wilson-Cowan population model to investigate fast (gamma band) oscillations generated by a local network of excitatory and inhibitory neurons. We modified the Wilson-Cowan equations to make them more physiologically realistic by explicitly incorporating background state variables into the model. We found that the population response is strongly influenced by the background state. We apply the model to reproduce the modulation of gamma rhythms by theta rhythms as has been observed in animal models and human ECoG and EEG studies. The concept of a dynamic background state presented here using the Wilson-Cowan model can be readily applied to incorporate top-down modulation in more detailed models of specific cortical systems.