Intracortical connections are not required for oscillatory activity in the visual cortex

Abstract

Synchronized oscillatory discharge in the visual cortex has been proposed to underlie the linking of retinotopically disparate features into perceptually coherent objects. These proposals have largely relied on the premise that the oscillations arise from intracortical circuitry. However, strong oscillations within both the retina and the lateral geniculate nucleus (LGN) have been reported recently. To evaluate the possibility that cortical oscillations arise from peripheral pathways, we have developed two plausible modeis of Single cell oscillatory discharge that specifically exclude intracortical networks. In the first model, cortical oscillatory discharge near 50 Hz in frequency arises from the integration of Signals from strongly oscillatory cells within the LGN. The model also predicts the incidence of 50-Hz oscillatory cells within the cortex. Oscillatory discharge around 30 Hz is explained in a second model by the presence of intrinsically oscillatory cells within cortical layer 5. Both modeis generate spike trains whose power spectra and mean firing rates are in close agreement with experimental observations of simple and complex cells. Considered together, the two modeis can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these modeis is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these modeis rely on intrinsic stimulus-independent oscillators within the retina and cortex, the results further suggest that oscillatory activity within the cortex is not necessarily associated with the processing of high-order visual information.