Nonlinear Y-like receptive fields in the early visual cortex: An intermediate stage for building cue-invariant receptive fields from subcortical Y cells.

Many of the neurons in early visual cortex are selective for orientation of boundaries defined by first-order (luminance) as well as second-order (contrast, texture) cues. The neural circuit mechanism underlying this selectivity is still unclear, but some studies have proposed that it emerges from spatial nonlinearities of subcortical Y cells.In order to understand how inputs from the Y cell pathway might be pooled to generate cue-invariant receptive fields, we recorded visual responses from single neurons in cat Area 18 using linear multi-electrode arrays. We measured responses to drifting and contrast-reversing luminance gratings as well as contrast-modulation gratings.We found that a large fraction of these neurons have non-oriented responses to gratings, similar to those of subcortical Y cells - they respond at the second harmonic (F2) to high spatial frequency contrast-reversing gratings and at the first harmonic (F1) to low spatial frequency drifting gratings ("Y-cell signature"). For a given neuron, spatial frequency tuning for linear (F1) and nonlinear (F2) response is quite distinct, similar to orientation-selective cue-invariant neurons. Also, these neurons respond to contrast modulation (CM) gratings with selectivity for the carrier (texture) spatial frequency and, in some cases, orientation. Their receptive field properties suggest that they could serve as building blocks for orientation selective cue-invariant neurons. We propose a circuit model that combines ON- and OFF-centre cortical Y-like cells in an unbalanced push-pull manner, to generate orientation selective cue-invariant receptive fields.

SIGNIFICANCE STATEMENT: A significant fraction of neurons in early visual cortex have specialized receptive fields that allow them to selectively respond to orientation of boundaries invariant of the cue (luminance, contrast, texture, motion) that defines them. However the neural mechanism to construct such versatile receptive fields remains unclear. Using multielectrode recording we found a large fraction of neurons in early visual cortex with receptive fields not selective for orientation, that have spatial nonlinearities like those of subcortical Y cells. These are strong candidates for building cue-invariant orientation selective neurons - we present a neural circuit model that pools such neurons in an imbalanced "push-pull" manner, to generate orientation-selective cue-invariant receptive fields.