Spatial frequency tuning of orientation-discontinuity-sensitive corticofugal feedback to the cat lateral geniculate nucleus

1. The influence of spatial frequency on the inhibitory component of the effects mediated by feedback from the visual cortex has been examined in X and Y cells in the A laminae of the feline dorsal lateral geniculate nucleus (dLGN). Experiments utilized a concentric, bipartite visual stimulus centred over the receptive fields of the cells studied. The responses of dLGN cells to selective stimulation of receptive field centre (with the inner window) were compared with those to stimulation of centre and surround mechanisms (both inner and outer window), with the stimuli either in or out of orientation alignment. 2. With these same stimuli, layer VI cells in the visual cortex showed a marked increase in response magnitude when the inner and outer components of the stimulus were in orientation alignment, and presented at the preferred orientation. In the case of dLGN X and Y cells we observed an enhancement of the surround antagonism of the centre response when the inner and outer sections of the stimulus were in orientation alignment. 3. The effects of varying spatial frequency on these responses were examined in dLGN cells in the presence of corticofugal feedback. With the stimulus sections in orientation alignment, surround stimulation produced a powerful and significant reduction in the response to stimulation of centre mechanism alone with the most marked effects for stimuli in the range 0.1-0.85 cycles per degree (c.p.d.). The reduction produced by surround stimulation in the range 0.1-0.5 c.p.d. was notably more potent in X cells than in Y cells. 4. The responses to the same stimuli were examined in dLGN cells with the corticofugal feedback inactivated. Comparison of data from cells studied with and without feedback revealed a significant decrease in surround-mediated attenuation of the centre response in Y cells for spatial frequencies in the range 0.1-0.85 c.p.d. For X cells the decrease in strength of the surround antagonism was also clear and significant but only seen in the range 0.1-0.5 c.p.d. 5. The influence of the orientation alignment of inner and outer stimulus sections revealed a marked difference between cells studied with and without feedback. In the presence of feedback fully aligned stimuli enhanced surround antagonism of centre responses for spatial frequencies in the range 0.1-0.5 c.p.d., in X and Y cells. In the absence of corticofugal feedback this alignment effect was essentially eliminated. 6. These data show that surround antagonism of the centre response is influenced by orientation alignment of the stimulus sections at low spatial frequencies and in the presence of corticofugal feedback. They support a cortically driven enhancement of the inhibitory mechanisms reinforcing surround mechanisms in the dLGN. The propose that feedback enhances a low spatial frequency cut-off in the dLGN, that this effect is maximal for a continuous iso-orientated contour, but diminished whenever there is an orientation discontinuity. The hyperpolarizing influence underlying this effect may contribute to the recently described synchronizing influence of the direct corticofugal contacts onto relay cells. We suggest feedback of the cortical level of analysis refines the transfer of the visual input at geniculate level in a stimulus-context-dependent fashion.