Form-cue Invariant Second-order Neuronal Responses To Contrast Modulation In Primate Area V2

Our rich perception of the complex mixtures of objects and surfaces comprising our everyday world is one of the most remarkable achievements of the human brain. A key early step in the required neural processing is separation of the retinal image into regions corresponding to distinct surfaces of different objects. In natural images we can effortlessly perform such figure-ground segmentation of borders defined by differences in a variety of local image properties ("cues"), e.g. differences in luminance, colour, contrast, or texture. This segmentation process necessarily precedes higher-level visual functions such as object recognition, and is fundamentally important to normal visual perception. Specific impairments of such boundary perception have been psychophysically demonstrated in young children, as a function of aging, and in clinical anomalies such as amblyopia. Thus the neural mechanisms underlying perception of these stimuli are significant and important for both basic and clinical vision science.In the mammalian visual system, the specific neuronal representation of these boundaries first occurs in the primary visual cortex. Neural mechanisms for detecting luminance and color boundaries have been well-described in primates, but it remains unclear how the brain is able to solve the much more challenging problem of segregating image regions differing in texture or contrast, so called "second-order" processing5. Neurons responding to such stimuli have been demonstrated and quantitatively analyzed in the cat in early visual cortex areas17&18, with rigorous control experiments to guard against possible artifacts. Neuronal responses to such boundaries have also been reported in primate visual cortex, but these studies have all been sorely lacking in (a) quantitative analysis of the neural mechanisms, and (b) any convincing controls for stimulus artifacts, which are potentially more likely in primates than in cats (see below). This is an especially serious worry for primates, whose much higher contrast sensitivity may afford more possibility of response to small demodulation artifacts. Neuronal responses to illusory contours can also be artifactual, in a different way:abutting gratings have many local physical luminance boundaries along the border at each of the bar terminations, which could be sensed by linearly summating neurons. This is also a more serious issue for primates, which have much smaller receptive fields than cats. While the cat has proven an excellent animal model system for exploring the neural basis of second-order processing, it is essential that we extend this knowledge to primates. The macaque monkey has become the standard animal model to closely match the human visual system.In this study we studied detection of moving luminance-or texture-defined boundaries by visual cortex neurons in the macaque monkey using single unit extracellular recording in macaque V2, an early visual cortical area known to exhibit more complex processing. We used a rich variety of analytically powerful stimuli (sinewave gratings, contrast envelopes, texture borders) to separate genuine responses from artifacts and analyze underlying mechanisms. We adopted a protocol to search for and characterize neuronal responses similar to that previously used successfully in the cat, i.e. first using responses to luminance-defined stimuli as a guide to likely modulation pattern parameters, with systematic testing of carrier parameters to find a neuron’s optimal CM stimulus. We find that a substantial fraction of V2cells show highly specific responses to contrast modulations, with carrier-tuning that rules out an early nonlinearity. These responses are also form-cue invariant, and with high ratios of carrier to modulation spatial frequency.Our results suggest that "second-order" variations could be detected by neurons in primate V2, and directly provide plausible neural substrates for human psychophysics of second-order processing. The results will provide a crucial "missing link" between the existing cat neurophysiology and human visual psychophysics.