Precisely Synchronized Oscillatory Firing Patterns Require Electroencephalographic Activation

Neuronal response synchronization with millisecond precision has been proposed to serve feature binding in vision and should therefore, like visual experience, depend on central states. Here we test this hypothesis by examining the occurrence and strength of response synchronization in areas 17 and 18 of anesthetized cats as a function of central states. These were assessed from the frequency content of the electroencephalogram, low power in the delta and high power in the gamma frequency ranges (here 20-70 Hz) being considered as a signature of activated states. We evaluated both spontaneous state changes and transitions induced by electrical stimulation of the mesencephalic reticular formation. During states of low central activation, visual responses were robust but lacked signs of precise synchronization. At intermediate levels of activation, responses became synchronized and exhibited an oscillatory patterning in the range of 70-105 Hz. At higher levels of activation, a different pattern of response synchronization and oscillatory modulation appeared, oscillation frequency now being in the range of 20-65 Hz. The strength of response synchronization and oscillatory modulation in the 20-65 Hz range increased with further activation and was associated with a decrease in oscillation frequency. We propose that the oscillatory patterning in the 70-105 Hz range is attributable to oscillatory retinothalamic input and that a minimal level of activation is necessary for cortical neurons to follow this oscillatory pattern. In contrast, the synchronization of responses at oscillation frequencies in the 20-65 Hz range appears to result from intracortical synchronizing mechanisms, which become progressively more effective as central activation increases. Surprisingly, enhanced synchronization and oscillatory modulation in the gamma frequency range were not associated with consistent increases in response amplitude, excluding a simple relation between central activation and neuronal discharge rate. The fact that intracortical synchronizing mechanisms are particularly effective during states of central activation supports the hypothesis that precise synchronization of responses plays a role in sensory processing.