Oscillatory discharge in the visual system: Does it have a functional role?

1. The discharge of individual neurons in the visual cortex and lateral geniculate nucleus (LGN) of anesthetized and paralyzed cats and kittens was examined for the presence of oscillatory activity. Neural firing was evoked through the monoptic or dichoptic presentation of drifting gratings and random sequences of flashed bars. The degree to which different oscillatory frequencies were present in neural discharge was quantified by computation of the power spectra of impulse train responses. 2. Action potentials from single cells were recorded extracellularly and isolated on the basis of amplitude. Receptive-field properties of the neurons under study were characterized initially by their discharge in response to gratings of sinusoidal luminance. By varying orientation and spatial frequency, optimal stimulus characteristics were determined. Oscillation analysis was performed on spike trains acquired during repeated presentations of the optimal stimulus by identification of power spectra peaks in the frequency range of rhythmic potentials observed in electroencephalograph studies (30-80 Hz). The amplitude and frequency of the largest peak in this range was used to characterize oscillatory strength and frequency. All discharge in which the peak amplitude exceeded the high-frequency noise by a factor > 1.5 was classified as oscillatory. 3. Of the 342 cortical cells examined, 147 cells displayed oscillatory activity in the 30 to 80-Hz range during portions of their visual response. Sixty out of 169 simple cells, 82 out of 166 complex cells, and 5 out of 7 special complex cells exhibited oscillations. There was no laminar bias in the distribution of oscillatory cells; the proportions of oscillatory cells were similar in all layers. All oscillatory discharge was variable with respect to frequency and strength between successive presentations of the same optimal stimulus. In as little as 10 s, for example, peak frequencies shifted by a factor of two. For many cells, these trial-to-trial variations obscured detectable oscillations when all trials were averaged together. 4. The potential role of neuronal maturation in the generation of oscillatory activity was investigated by studying neuronal responses from kittens at 4 wk postnatal. Of the 80 kitten cells studied, 27 exhibited oscillatory discharge. Although oscillations in the kitten visual cortex spanned the same frequency range as that seen in the adult, oscillations in the midfrequency range (36-44 Hz) are more common in the adult cortex. 5. To explore the possibility that oscillations might play a functional role in vision, we investigated the dependence of oscillations on different stimulus parameters. Responses to dichoptically presented drifting gratings showed no relationship between binocular interactions and oscillatory discharge: oscillations were just as likely to occur with nonoptimal as with optimal binocular stimuli. For 98 binocular cells that exhibited oscillatory discharge, monocular and binocular responses were compared. Sixty-one of these cells exhibited oscillatory discharge under both monocular and binocular stimulation. The numbers of cells that oscillated solely under binocular stimulation or solely under monocular stimulation were approximately equal (18 and 19, respectively). Among the 61 cells that oscillated with both monocular and binocular stimuli, about one-half showed stronger oscillations for binocular stimulation.