Frequency-doubling in the early visual system underlies sensitivity to second-order stimuli

Abstract

There are two primary visual cortical areas in the cat, each receiving a direct LGN projection. Area 17 neurons are described reasonably well by linear filters selective for the orientation and spatiotemporal frequencies of stimuli. Area 18 neurons are thought to be analogous except that they are selective for lower spatial and higher temporal frequencies. However, about half of Area 18 neurons possess a nonlinearity that makes them sensitive to beat frequencies and other second-order stimuli. Because second-order responsive neurons are tuned for the orientation of the high spatial frequency carrier of a beat stimulus, it has been argued that this selectivity arises from a nonlinear combination of Area 17 inputs (Mareschal & Baker, 1998). Alternatively, this selectivity may originate from their LGN inputs, Y-cells. Consistent with this, Y-cells are responsive to low spatial frequencies but also show frequency-doubled responses to contrast-reversing stimuli at the high spatial frequencies used to construct second-order stimuli. Furthermore, the activity of retinal ganglion Y-cells modulates at the temporal frequency of second-order stimuli (Demb et al., 2001). To date however, it has been assumed, but not tested, that Y-cell tuning properties cannot account for the orientation selectivity of second-order responses in Area 18. We asked if LGN responses to second-order stimuli can account for those in Area 18. Our results indicate that while X-cells are unresponsive to these stimuli, Y-cells behave similarly to Area 18 neurons. First, Y-cells show tuning for the orientation of the carrier of a beat stimulus. Second, the preferred temporal frequency and cut-off is greater for drifting sinusoidal gratings than for the envelope of a beat. Third, the temporal frequency tuning of the carrier resembles that of Area 18 neurons. Together, these findings suggest that the frequency-doubling nonlinearity of Y-cells is sufficient to account for second-order responses in cat Area 18.