Yiliang Lu

Equivalent Representation of Real and Illusory Contours in Macaque V4

The cortical processing of illusory contours provides a unique window for exploring the brain mechanisms underlying visual perception. Previous electrophysiological single-cell recordings demonstrate that a subgroup of cells in macaque V1 and V2 signal the presence of illusory contours, whereas recent human brain imaging studies reveal higher-order visual cortices playing a central role in illusory figure processing. It seems that the processing of illusory contours/figures may engage multiple cortical interactions between hierarchically organized processing stages in the ventral visual pathway of primates. However, it is not yet known in which brain areas illusory contours are represented in the same manner as real contours at both the population and single-cell levels. Here, by combining intrinsic optical imaging in anesthetized rhesus macaques with single-cell recordings in awake ones, we found a complete overlap of orientation domains in visual cortical area V4 for processing real and illusory contours. In contrast, the orientation domains mapped in early visual areas V1 and V2 mainly encoded the local physical stimulus features inducing the subjective perception of global illusory contours. Our results indicate that real and illusory contours are encoded equivalently by the same functional domains in V4, suggesting that V4 is a key cortical locus for integration of local features into global contours.

Orientation-Cue Invariant Population Responses to Contrast-Modulated and Phase-Reversed Contour Stimuli in Macaque V1 and V2

Visual scenes can be readily decomposed into a variety of oriented components, the processing of which is vital for object segregation and recognition. In primate V1 and V2, most neurons have small spatio-temporal receptive fields responding selectively to oriented luminance contours (first order), while only a subgroup of neurons signal non-luminance defined contours (second order). So how is the orientation of second-order contours represented at the population level in macaque V1 and V2? Here we compared the population responses in macaque V1 and V2 to two types of second-order contour stimuli generated either by modulation of contrast or phase reversal with those to first-order contour stimuli. Using intrinsic signal optical imaging, we found that the orientation of second-order contour stimuli was represented invariantly in the orientation columns of both macaque V1 and V2. A physiologically constrained spatio-temporal energy model of V1 and V2 neuronal populations could reproduce all the recorded population responses. These findings suggest that, at the population level, the primate early visual system processes the orientation of second-order contours initially through a linear spatio-temporal filter mechanism. Our results of population responses to different second-order contour stimuli support the idea that the orientation maps in primate V1 and V2 can be described as a spatial-temporal energy map.

Focal Gain Control of Thalamic Visual Receptive Fields by Layer 6 Corticothalamic Feedback

The projections between the thalamus and primary visual cortex (V1) are a key reciprocal neural circuit, relaying retinal signals to cortical layers 4 & 6 while being simultaneously regulated by massive layer 6 corticothalamic feedback. Effectively dissecting the influence of this corticothalamic feedback circuit in higher mammals remains a challenge for vision research. By pharmacologically increasing the focal gain of visually driven layer 6 responses of cat V1 in a controlled fashion, we examined the effects of such focal cortical changes on the response amplitudes and spatial structure of the receptive fields (RFs) of individual dorsal lateral geniculate nucleus (dLGN) cells. We found that enhancing visually driven cortical feedback could facilitate or suppress the overall responses of dLGN cells, and such an effect was linked to the orientation preference of the cortical neuron. Related to these selective retinotopic gain changes, enhanced feedback induced the RFs of dLGN cells to expand, contract or shift their spatial focus. Our results provide further evidence for a functional mechanism through which the cortex can selectively gate visual information flow from the thalamus back to the visual cortex.

Breaking cover: neural responses to slow and fast camouflage-breaking motion

Primates need to detect and recognize camouflaged animals in natural environments. Camouflage-breaking movements are often the only visual cue available to accomplish this. Specifically, sudden movements are often detected before full recognition of the camouflaged animal is made, suggesting that initial processing of motion precedes the recognition of motion-defined contours or shapes. What are the neuronal mechanisms underlying this initial processing of camouflaged motion in the primate visual brain? We investigated this question using intrinsic-signal optical imaging of macaque V1, V2 and V4, along with computer simulations of the neural population responses. We found that camouflaged motion at low speed was processed as a direction signal by both direction- and orientation-selective neurons, whereas at high-speed camouflaged motion was encoded as a motion-streak signal primarily by orientation-selective neurons. No population responses were found to be invariant to the camouflage contours. These results suggest that the initial processing of camouflaged motion at low and high speeds is encoded as direction and motion-streak signals in primate early visual cortices. These processes are consistent with a spatio-temporal filter mechanism that provides for fast processing of motion signals, prior to full recognition of camouflage-breaking animals.

Asymmetries of Dark and Bright Negative Afterimages Are Paralleled by Subcortical ON and OFF Post-Stimulus Responses

Humans are more sensitive to luminance decrements than increments, as evidenced by lower thresholds and shorter latencies for dark stimuli. This asymmetry is consistent with results of neurophysiological recordings in dorsal lateral geniculate nucleus (dLGN) and primary visual cortex (V1) of cat and monkey. Specifically, V1 population responses demonstrate that darks elicit higher levels of activation than brights, and the latency of OFF responses in dLGN and V1 is shorter than that of ON responses. The removal of a dark or bright disc often generates the perception of a negative afterimage, and here we ask whether there also exist asymmetries for negative afterimages elicited by dark and bright discs. If so, do the poststimulus responses of subcortical ON and OFF cells parallel such afterimage asymmetries? To test these hypotheses, we performed psychophysical experiments in humans and single-cell/S-potential recordings in cat dLGN. Psychophysically, we found that bright afterimages elicited by luminance decrements are stronger and last longer than dark afterimages elicited by luminance increments of equal sizes. Neurophysiologically, we found that ON cells responded to the removal of a dark disc with higher firing rates that were maintained for longer than OFF cells to the removal of a bright disc. The ON and OFF cell asymmetry was most pronounced at long stimulus durations in the dLGN. We conclude that subcortical response strength differences between ON and OFF channels parallel the asymmetries between bright and dark negative afterimages, further supporting a subcortical origin of bright and dark afterimage perception. SIGNIFICANCE STATEMENT Afterimages are physiological aftereffects following stimulation of the eye, the study of which helps us to understand how our visual brain generates visual perception in the absence of physical stimuli. We report, for the first time to our knowledge, asymmetries between bright and dark negative afterimages elicited by luminance decrements and increments, respectively. Bright afterimages are stronger and last longer than dark afterimages. Subcortical neuronal recordings of poststimulus responses of ON and OFF cells reveal similar asymmetries with respect to response strength and duration. Our results suggest that subcortical differences between ON and OFF channels help explain intensity and duration asymmetries between bright and dark afterimages, supporting the notion of a subcortical origin of bright and dark afterimages.

The Neural Mechanism of Direction- and Orientation-Selective Neurons for Processing Direction, Speed, and Axis of Motion in Early Visual Cortices

Visual motion is fundamentally different from physical motion, because the former represents sequential retinotopic neuronal activations in time generated by a physical moving object. Traditionally, cortical direction-selective neurons are regarded as motion detector while orientation-selective neurons as contour detector. However, orientation-selective neurons also respond rigorously to motion stimuli. What is then the common neural mechanism underlying early motion processing in high mammalians? Here we demonstrate that motion trajectory only at low speed was encoded primarily as direction signal by both direction- and orientation-selective neurons preferring that motion direction, but at high speed, other groups of direction- and orientation-selective neurons with perpendicular preferences were activated to encode the motion trajectory as motion-axis information. Thus, depending on the motion speed, the combined processing of motion direction and axis by neurons with orthogonal direction and orientation preferences may serve as a fundamental principle of visual motion processing in early visual areas of high mammalians.

The Application of Spatiotemporal Energy Model in the Simulation of Population Responses in Early Visual Cortices

The early visual cortices (V1 and V2) are traditionally regarded as local feature detectors or filters of spatiotemporal components while higher visual areas as centers for global feature or object recognition in high mammalians. Natural scenes are complicated, thus synthesized visual stimuli are often composed of various local and global visual cues. Here we propose that the spatiotemporal energy model could simulate the population responses to the local component of most visual stimulus in the early visual cortices. The population responses to stimuli of either luminance or contrast and texture modulations, recorded using intrinsic optical imaging in both V1 and V2 of macaques and cats, could be successfully predicted by the energy model. However, it failed to predict the population responses to other complex stimuli such as illusory and kinetic contours. These results illustrated the application and limitation of the spatiotemporal energy model in accounting for population responses in the early visual cortices.

Asymmetrical color filling-in from the nasal to the temporal side of the blind spot

The physiological blind spot, corresponding to the optic disk in the retina, is a relatively large (6 × 8°) area in the visual field that receives no retinal input. However, we rarely notice the existence of it in daily life. This is because the blind spot fills in with the brightness, color, texture, and motion of the surround. The study of filling-in enables us to better understand the creative nature of the visual system, which generates perceptual information where there is none. Is there any retinotopic rule in the color filling-in of the blind spot? To find out, we used mono-colored and bi-colored annuli hugging the boundary of the blind spot. We found that mono-colored annuli filled in the blind spot uniformly. By contrast, bi-colored annuli, where one half had a given color, while the other half had a different one, filled in the blind spot asymmetrically. Specifically, the color surrounding the nasal half typically filled in about 75% of the blind spot area, whereas the color surrounding the temporal half filled in only about 25%. This asymmetry was dependent on the relative size of the half rings, but not the two colors used, and was absent when the bi-colored annulus was rotated by 90°. Here, the two colors on the upper and lower sides of the blind spot filled in the enclosed area equally. These results suggest that the strength of filling-in decreases with distance from the fovea consistent with the decrease of the cortical magnification factor.