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

Abstract

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 phaseinvariant 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.

Nonlinear Y-Like Receptive Fields in the Early Visual Cortex: An Intermediate Stage for Building Cue-Invariant Receptive Fields from Subcortical Y Cells

“…This challenges previous ideas that firstand second-order cues are processed independently (Smith and Ledgeway, 1997) and that second-order cues are encoded in higher extrastriate areas (Smith et al, 1998;El-Shamayleh and Movshon, 2011;Pan et al, 2012;An et al, 2014). Previous studies have extensively analyzed the pooling of subcortical X-pathway inputs in cat Area 17 to generate simple cell (linear, Gabor-like) receptive fields with a "push-pull" combination of ON-and OFF-center cells (Ferster, 1988;Hirsch et al, 1998;Martinez et al, 2005). However, Area 18 receives a majority of its lateral geniculate nucleus (LGN) input from the nonlinear Y-pathway, and it is unclear how these inputs are combined to generate receptive fields with precise selectivity for first-order as well as second-order cues.…”

“…However, there have been some reports also finding a substantial fraction of LGN-like nonoriented receptive fields in the early mammalian visual cortex. For example, non-ori neurons have been found in primary visual cortex of macaque (Livingstone and Hubel, 1984;Ringach, 2002;Ringach et al, 2002), mouse (Bonin et al, 2011), and ferret (Chapman and Stryker, 1993), as well as in cat Area 17 (Dragoi et al, 2001;Hirsch et al, 2003). Earlier studies using single channel electrodes and barshaped search stimuli in cat Area 18 (Ferster and Jagadeesh, 1991;Mareschal and Baker, 1998a;Tanaka and Ohzawa, 2006) did not report nonoriented receptive fields.…”

“…For example, non-ori neurons have been found in primary visual cortex of macaque (Livingstone and Hubel, 1984;Ringach, 2002;Ringach et al, 2002), mouse (Bonin et al, 2011), and ferret (Chapman and Stryker, 1993), as well as in cat Area 17 (Dragoi et al, 2001;Hirsch et al, 2003). Earlier studies using single channel electrodes and barshaped search stimuli in cat Area 18 (Ferster and Jagadeesh, 1991;Mareschal and Baker, 1998a;Tanaka and Ohzawa, 2006) did not report nonoriented receptive fields. But a recent study (Talebi and Baker, 2016) in cat Area 18 using multichannel electrodes, in conjunction with post hoc data analysis (spike sorting) similar to ours, has reported a large proportion of nonoriented receptive fields estimated using system identification methods.…”

“…7B) that could generate cue-invariant orientation-selective receptive fields from responses of cortical Y-like cells. In this model, the responses of both ON-and OFF-center cortical neurons are combined in a "push-pull" manner (Ferster, 1988;Hirsch et al, 1998;Martinez et al, 2005): the ON subregions of an oriented receptive field receive excitatory input from ON-center cells and also inhibitory input from OFF-center cells, and vice versa for the OFF subregions. It is straightforward to see that this receptive field would be selective for the orientation of a luminance boundary.…”

“…A substantial fraction of neurons in the early visual cortex (Area 18) of cats respond in a cue-invariant manner to boundaries formed by first-order (luminance) or second-order (contrast, texture, motion) differences (Zhou and Baker, 1993;Tanaka and Ohzawa, 2006;Song and Baker, 2007;Gharat and Baker, 2012). Recently, neurons in the early visual cortex (V2) of nonhuman primates were also shown to respond cue invariantly to luminance-and contrast-defined boundaries (Li et al, 2014), with spatial selectivity to the carrier (texture) and envelope (modulator) of contrast boundaries that is very similar to previous findings in cat Area 18 (Mareschal andBaker, 1998a, 1999).…”