Mammalian striate and circumstriate cortical neurons have long been understood as coding spatially localized retinal luminance variations, providing a basis for computing motion, stereopsis, and contours from the retinal image. However, such perceptual attributes do not always correspond to the retinal luminance variations in natural vision. Recordings from area 17 and 18 neurons of the cat revealed a specialized nonlinear processing stream that responds to stimulus attributes that have no corresponding luminance variations. This nonlinear stream acts in parallel to the conventional luminance processing of single cortical neurons. The two streams were consistent in their preference for orientation and direction of motion but distinct in processing spatial variations of the stimulus attributes.

Object boundaries in the natural environment are often defined by changes in luminance; in other cases, however, there may be no difference in average luminance across the boundary, which is instead defined by more subtle 'second-order' cues, such as changes in the contrast of a fine-grained texture. The detection of luminance boundaries may be readily explained in terms of visual cortical neurons, which compute the linear sum of the excitatory and inhibitory inputs to different parts of their receptive field. The detection of second-order stimuli is less well understood, but is thought to involve a separate nonlinear processing stream, in which boundary detectors would receive inputs from many smaller subunits. To address this, we have examined the properties of cortical neurons which respond to both first- and second-order stimuli. We show that the inputs to these neurons are also oriented, but with no fixed orientational relationship to the neurons they subserve. Our results suggest a flexible mechanism by which the visual cortex can detect object boundaries regardless of whether they are defined by luminance or texture.

We have recorded electroretinographic (ERG) responses to grating patterns whose spatial, temporal, and contrast parameters were varied. The resultant evoked potential is dependent on spatial frequency and it exhibits a spatial band-pass characteristic. The peak frequency is dependent on retinal eccentricity. These findings are independent of temporal frequency, contrast, or mean luminance in the photopic range. These results suggest that the pattern ERG originates from a postreceptoral site.

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Temporal and spatial response to second-order stimuli in cat area 18. J. Neurophysiol. 80: 2811-2823, 1998. Approximately one-half of the neurons in cat area 18 respond to contrast envelope stimuli, consisting of a sinewave carrier whose contrast is modulated by a drifting sinewave envelope of lower spatial frequency. These stimuli should fail to elicit a response from a conventional linear neuron because they are designed to contain no spatial frequency components within the cell's luminance-defined frequency passband. We measured neurons' responses to envelope stimuli by varying both the drift rate and spatial frequency of the contrast modulation. These data were then compared with the same neurons' spatial and temporal properties obtained with luminance-defined sinewave gratings. Most neurons' responses to the envelope stimuli were spatially and temporally bandpass, with bandwidths comparable with those measured with luminance gratings. The temporal responses of these neurons (temporal frequency tuning and latency) were systematically slower when tested with envelope stimuli than with luminance gratings. The simplest kind of model that can accommodate these results is one having separate, parallel streams of bandpass processing for luminance and envelope stimuli.

A neurological patient (L.M.) suffering a specific loss of visual motion perception (Zihl et al., 1983) due to extrastriate cortical damage was studied using random dot "limited-lifetime" stimuli with a direction discrimination task. With a stimulus like that of Newsome and Pare (1988), the patient exhibited a severe deficit for motion perception, only being able to perform well for very high values of coherence. Different versions of the stimulus were employed to separate out the effects of limited lifetime versus the effects of additive noise as coherence was lowered. When all "signal" dots had a fixed, specified value of lifetime, and varying percentages of "noise" dots were added, the patient showed a profound deficit. In contrast, a stimulus consisting of no noise dots at all, and signal dots having fixed values of lifetime, revealed relatively good performance for surprisingly brief dot lifetimes. Thus, it is the presence of noisy, incoherent dot motion, rather than brief lifetimes, that causes such poor performance on the stimulus of Newsome and Pare (1988). Most surprising was the finding that the presence of even very small percentages of stationary noise dots was sufficient to disrupt totally direction discrimination of moving signal dots. The findings reported here suggest that one major role of extrastriate cortical processing might be the interpretation of stimuli that suffer from an impaired signal-to-noise ratio; the most commonly encountered form of "noise" would presumably be contamination by irrelevant directional spatio-temporal frequency components.

A study is reported of the perception of random-dot two-frame apparent motion in which the durations of each exposure and the interstimulus interval between them were varied. The results are largely consistent with the rule that, for optimal motion detection, a portion of each exposure must fall within the same time interval of about 40 ms. In addition, motion perception is separably dependent on the displacement from one exposure to the next and on the time interval between those exposures, rather than on the 'velocity' implied by their ratio.