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 models 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 models 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 models can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these models is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these models 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.

Gamma-range oscillations in backward-masking functions and their putative neural correlates.

“…A subset of neurons in the visual cortex of anesthetized cats respond to stimuli with gamma-range oscillations that can be synchronized within a few milliseconds between neighboring layers, columns, and areas (Gray & Singer, 1989a, 1989b; Eckhorn et al, 1988). The existence of these oscillations, at least in monkeys (Tovee & Rolls, 1992; Young, Tanaka, & Yamane, 1992), and their stimulus dependence (Ghose & Freeman, 1992, 1997) has been controversial. Based on recent studies that replicated and extended the earlier findings in cats and monkeys (including alert animals; e.g., Bringuier, Frégnac, Baranyi, Debanne, & Shulz, 1997; Gray & Viana Di Prisco, 1997; Livingstone, 1996; Maunsell & Gibson, 1992; Molotchnikoff & Shumikhina, 1996; Molotchnikoff, Shumikhina, & Moisan, 1996), it is likely that some data analysis issues may be at the root of the controversy.…”

Temporal Structure in the Input to Vision Can Promote Spatial Grouping

“…This skepticism exists for several reasons. Some have argued that synchronized activity may be an artifact that simply arises from the spiking behavior of retinal and/or thalamic cells unrelated to stimulus-driven phase locking (Ghose and Freeman 1997) or from the statistical properties of rapidly spiking cells (Shadlen and Movshon 1999). Others question whether the noisy spike trains from individual neurons possess the temporal fidelity for temporal patterning to be informationally relevant (Shadlen and Newsome 1998).…”