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 reco rded extracellularly and 76 intracellularly) in the primary visual cor tex of cats and kittens to characterize its origins and its stimulus d ependency. A new method for the detection of oscillations was develope d in order to maximize the range of detectable frequencies in both typ es of recordings. Three types of activity were examined: spontaneous b ackground activity, responses to intracellular current steps and visua l responses. 2. During spontaneous activity, persistent oscillatory ac tivity was very rare in both types of recordings. However, when intrac ellular 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 i nput normally masked at resting potential. 3. Patterns of firing activ ity in response to intracellular current steps allowed us to classify neurons as regular spiking, intrinsically bursting, and fast-spiking t ypes, as described in vitro. In the case of rhythmically firing cells, the spike frequency increased with the amount of injected current. Su bthreshold current-induced oscillations were rarely observed (2 out of 76 cells). 4. Visual stimulation elicited oscillations in one-third o f 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 an d complex cells and appeared to be more prominent at 5 and 6 weeks of age. 5. Intracellular recordings in bridge mode and voltage clamp reve aled that visually evoked oscillations were driven by synaptic activit y 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 valu e of the holding potential. 6. In fourteen intracellularly recorded ne urons, oscillations consisted of excitatory events that could be super imposed on a depolarizing or a hyperpolarizing slow wave. In two other neurons, visual responses consisted of excitatory and inhibitory even ts, alternating with a constant phase shift. 7. Drifting bars were muc h more efficient in evoking oscillatory responses than flashed bars. E xcept in three cells, the frequency of the oscillation did not depend on the physical characteristics of the stimulus that were tested (cont rast, 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. Alt hough it cannot be excluded that the dominant frequency of oscillation s might be related to the type of anaesthetics used, no correlation wa s found between local EEG and the oscillatory activity elicited by vis ual stimulation. 9. The conclude that the oscillations observed in the present work are generated by synaptic activity It is likely that the y represent an important mode of transmission in sensory processing, r esulting from periodic packets of synchronized activity propagated acr oss recurrent circuits. Their relevance to perceptual binding is furth er discussed.