Phase-Dependent Interactions in Visual Cortex to Combinations of First- and Second-Order Stimuli.

A fundamental task of the visual system is to extract figure-ground boundaries between objects, which are often defined, not only by differences in luminance, but also by "second-order" contrast or texture differences. Responses of cortical neurons to both first- and second-order patterns have been studied extensively, but only for responses to either type of stimulus in isolation. Here, we examined responses of visual cortex neurons to the spatial relationship between superimposed periodic luminance modulation (LM) and contrast modulation (CM) stimuli, the contrasts of which were adjusted to give equated responses when presented alone. Extracellular single-unit recordings were made in area 18 of the cat, the neurons of which show responses to CM and LM stimuli very similar to those in primate area V2 (Li et al., 2014). Most neurons showed a significant dependence on the relative phase of the combined LM and CM patterns, with a clear overall optimal response when they were approximately phase aligned. The degree of this phase preference, and the contributions of suppressive and/or facilitatory interactions, varied considerably from one neuron to another. Such phase-dependent and phase-invariant responses were evident in both simple- and complex-type cells. These results place important constraints on any future model of the underlying neural circuitry for second-order responses. The diversity in the degree of phase dependence between LM and CM stimuli that we observed could help to disambiguate different kinds of boundaries in natural scenes. SIGNIFICANCE STATEMENT: Many visual cortex neurons exhibit orientation-selective responses to boundaries defined by differences either in luminance or in texture contrast. Previous studies have examined responses to either type of boundary in isolation, but here we measured systematically responses of cortical neurons to the spatial relationship between superimposed periodic luminance-modulated (LM) and contrast-modulated (CM) stimuli with contrasts adjusted to give equated responses. We demonstrate that neuronal responses to these compound stimuli are highly dependent on the relative phase between the LM and CM components. Diversity in the degree of such phase dependence could help to disambiguate different kinds of boundaries in natural scenes, for example, those arising from surface reflectance changes or from illumination gradients such as shading or shadows.