Synaptic origin and stimulus dependency of neuronal oscillatory activity in the primary visual cortex of the cat

1. We have studied the oscillatory activity of single neurons (91 recorded extracellularly and 76 intracellularly) in the primary visual cortex of cats and kittens to characterize its origins and its stimulus dependency. A new method for the detection of oscillations was developed in order to maximize the range of detectable frequencies in both types of recordings. Three types of activity were examined: spontaneous background activity, responses to intracellular current steps and visual responses. 2. During spontaneous activity, persistent oscillatory activity was very rare in both types of recordings. However, when intracellular records were made using KCl-filled micropipettes, spontaneous activity appeared rhythmic and contained repeated depolarizing events at a variety of frequencies, suggestive of tonic periodic inhibitory input normally masked at resting potential. 3. Patterns of firing activity in response to intracellular current steps allowed us to classify neurons as regular spiking, intrinsically bursting, and fast-spiking types, as described in vitro. In the case of rhythmically firing cells, the spike frequency increased with the amount of injected current. Subthreshold current-induced oscillations were rarely observed (2 out of 76 cells). 4. Visual stimulation elicited oscillations in one-third of the neurons (55 out of 167), predominantly in the 7-20 Hz frequency range in 93% of the cases. Rhythmicity was observed in both simple and complex cells, and appeared to be more prominent at 5 and 6 weeks of age. 5. Intracellular recordings in bridge mode and voltage clamp revealed that visually evoked oscillations were driven by synaptic activity and did not depend primarily on the intrinsic properties of recorded neurons. Hyperpolarizing the membrane led to an increase in the size of the rhythmic depolarizing events without a change in frequency. In voltage-clamped cells, current responses showed large oscillations at the same frequency as in bridge mode, independently of the actual value of the holding potential. 6. In fourteen intracellularly recorded neurons, oscillations consisted of excitatory events that could be superimposed on a depolarizing or a hyperpolarizing slow wave. In two other neurons, visual responses consisted of excitatory and inhibitory events, alternating with a constant phase shift. 7. Drifting bars were much more efficient in evoking oscillatory responses than flashed bars. Except in three cells, the frequency of the oscillation did not depend on the physical characteristics of the stimulus that were tested (contrast, orientation, direction, ocularity and position in the receptive field). No significant correlation was found between the intensity of the visual response and the strength of the rhythmic component. 8. Although it cannot be excluded that the dominant frequency of oscillations might be related to the type of anaesthetics used, no correlation was found between local EEG and the oscillatory activity elicited by visual stimulation. 9. We conclude that the oscillations observed in the present work are generated by synaptic activity. It is likely that they represent an important mode of transmission in sensory processing, resulting from periodic packets of synchronized activity propagated across recurrent circuits. Their relevance to perceptual binding is further discussed.