Hyperacuity in cat retinal ganglion cells.

Cat X retinal ganglion cells that can resolve sine gratings of only 2.5 cycles per degree can nevertheless respond reliably to displacements of a grating of approximately 1 minute of arc. This is a form of hyperacuity comparable in magnitude to that seen in human vision. A theoretical analysis of this form of hyperacuity reveals it to be a result of the high gain and low noise of ganglion cells. The hyperacuity expected for the best retinal ganglion cells is substantially better than that observed in behavioral experiments. Thus the brain, rather than improving on the retinal signal-to-noise ratio by pooling signals from many ganglion cells, is unable to make use of all the hyperacuity information present in single ganglion cell responses.

Enhanced perception of illusory contours in the lower versus upper visual hemifields.

The visual world consciously perceived is very different from the spatial array of photo-receptor activation present on our retinae; it is composed of segregated surfaces, organized into distinct objects. An important component of this organizational process, the segmentation of an image into figures and background, is shown to be performed much better in the lower visual field. This finding is demonstrated by the performance in two tasks that involve the perception of illusory contours. This asymmetry indicates a neural specialization that may be related to the anatomical discontinuity along the representation of the horizontal meridian in extrastriate visual cortex.

The spatial transformation of color in the primary visual cortex of the macaque monkey.

Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.

Contrast's effect on spatial summation by macaque V1 neurons.

Stimulation outside the receptive field of a primary visual cortical (V1) neuron reveals intracortical neural interactions. However, previous investigators implicitly or explicitly considered the extent of cortical spatial summation and, therefore, the size of the classical receptive field to be fixed and independent of stimulus characteristics or of surrounding context. On the contrary, we found that the extent of spatial summation in macaque V1 neurons depended on contrast, and was on average 2.3-fold greater at low contrast. This adaptive increase in spatial summation at low contrast was seen in cells throughout V1 and was independent of surround inhibition.

Retinal physiology: adapting to the changing scene.

The retina needs to process visual information under a wide range of conditions, a feat facilitated by gain controls. Recent results have provided new insights into one such gain control, which enables the retina to adapt to wide variations in the level of contrast in the visual scene.

Abrupt learning and retinal size specificity in illusory-contour perception.

BACKGROUND: In behavioral studies of learning, a distinction is commonly made between gradual and abrupt improvements in performance. The learning of perceptual and motor skills is often characterized by gradual, incremental improvement, and is found not to generalize over stimulus manipulations such as changes in the size or location of the retinal image. In contrast, marked improvement in performance can occur suddenly - a phenomenon which has been termed 'insight'. Consequently, the brain mechanisms subserving the two types of learning are commonly thought of as distinct. Here, we examine learning of a perceptual task in which improvement appears to exhibit characteristics of both gradual and abrupt learning. RESULTS: We describe experiments on illusory-contour perception in which the observers underwent an abrupt, dramatic improvement in performance, resembling an incident of insight. At the same time, however, the phenomenon showed a degree of stimulus-specificity that was previously thought to characterize incremental, gradual learning. The improvement was triggered only by specific visual stimuli, whereas other, quite similar, stimuli were found to be ineffective for training; the learning did not generalize to a new retinal image size, and re-training was necessary for different-sized images. CONCLUSIONS: The juxtaposition of abrupt and stimulus-specific learning that we observed suggests that the distinction between the two forms of learning needs to be revised. Rather than postulating two distinct mechanisms, incremental and insightful learning need to be addressed within a single framework. In particular, the findings suggest that learning may involve interactions between multiple levels of representations of the stimulus.

New perspectives on the mechanisms for orientation selectivity.

Since the discovery of orientation selectivity by Hubel and Wiesel, the mechanisms responsible for this remarkable operation in the visual cortex have been controversial. Experimental studies over the past year have highlighted the contribution of feedforward thalamo-cortical afferents, as proposed originally by Hubel and Wiesel, but they have also indicated that this contribution alone is insufficient to account for the sharp orientation tuning observed in the visual cortex. Recent advances in understanding the functional architecture of local cortical circuitry have led to new proposals for the involvement of intracortical recurrent excitation and inhibition in orientation selectivity. Establishing how these two mechanisms work together remains an important experimental and theoretical challenge.

How simple cells are made in a nonlinear network model of the visual cortex.

Simple cells in the striate cortex respond to visual stimuli in an approximately linear manner, although the LGN input to the striate cortex, and the cortical network itself, are highly nonlinear. Although simple cells are vital for visual perception, there has been no satisfactory explanation of how they are produced in the cortex. To examine this question, we have developed a large-scale neuronal network model of layer 4Calpha in V1 of the macaque cortex that is based on, and constrained by, realistic cortical anatomy and physiology. This paper has two aims: (1) to show that neurons in the model respond like simple cells. (2) To identify how the model generates this linearized response in a nonlinear network. Each neuron in the model receives nonlinear excitation from the lateral geniculate nucleus (LGN). The cells of the model receive strong (nonlinear) lateral inhibition from other neurons in the model cortex. Mathematical analysis of the dependence of membrane potential on synaptic conductances, and computer simulations, reveal that the nonlinearity of corticocortical inhibition cancels the nonlinear excitatory input from the LGN. This interaction produces linearized responses that agree with both extracellular and intracellular measurements. The model correctly accounts for experimental results about the time course of simple cell responses and also generates testable predictions about variation in linearity with position in the cortex, and the effect on the linearity of signal summation, caused by unbalancing the relative strengths of excitation and inhibition pharmacologically or with extrinsic current.

Fluctuations of the impulse rate in Limulus eccentric cells.

Fluctuations in the discharge of impulses were studied in eccentric cells of the compound eye of the horseshoe crab, Limulus polyphemus. A theory is presented which accounts for the variability in the response of the eccentric cell to light. The main idea of this theory is that the source of randomness in the impulse rate is "noise" in the generator potential. Another essential aspect of the theory is that the process which transforms the generator potential "noise" into the impulse rate fluctuations may be treated as a linear filter. These ideas lead directly to Fourier analysis of the fluctuations. Experimental verification of theoretical predictions was obtained by calculation of the variance spectrum of the impulse rate. The variance spectrum of the impulse rate is shown to be the filtered variance spectrum of the generator potential.

Effects of lateral inhibition on fluctuations of the impulse rate.

Inhibition from neighboring eccentric cells has an effect on the variability of firing of a given eccentric cell. The reduction in the average impulse rate which is caused by inhibition decreases the variance of the impulse rate. However, this reduction of the average rate increases the coefficient of variation of the impulse rate. Inhibitory synaptic noise should add to the low frequency portion of the variance spectrum of the impulse rate. This occurs because of the slow time course of inhibitory synaptic potentials. As a consequence, inhibition decreases the signal-to-noise ratio for low frequency modulated stimuli.

Spatial and temporal properties of luminosity horizontal cells in the turtle retina.

Luminosity horizontal cells in the turtle retina respond approximately linearly to visual stimuli with contrast levels spanning a large part of the physiological range. We characterized the response properties of these cells under conditions of low photopic background illumination by measuring their spatial and temporal frequency transfer functions. Our experimental results indicate in two ways that, under these conditions, feedback from luminosity horizontal cells to cones does not play a major role in the mechanisms underlying the spatial and temporal tuning of horizontal cell responses. First, the shape of the spatial transfer function depended only weakly on the temporal frequency with which it was measured. Second, the shape of the temporal transfer function depended only weakly on the spatial frequency with which it was measured.

Receptive field mechanisms of cat X and Y retinal ganglion cells.

We investigated receptive field properties of cat retinal ganglion cells with visual stimuli which were sinusoidal spatial gratings amplitude modulated in time by a sum of sinusoids. Neural responses were analyzed into the Fourier components at the input frequencies and the components at sum and difference frequencies. The first-order frequency response of X cells had a marked spatial phase and spatial frequency dependence which could be explained in terms of linear interactions between center and surround mechanisms in the receptive field. The second-order frequency response of X cells was much smaller than the first-order frequency response at all spatial frequencies. The spatial phase and spatial frequency dependence of the first-order frequency response in Y cells in some ways resembled that of X cells. However, the Y first-order response declined to zero at a much lower spatial frequency than in X cells. Furthermore, the second-order frequency response was larger in Y cells; the second-order frequency components became the dominant part of the response for patterns of high spatial frequency. This implies that the receptive field center and surround mechanisms are physiologically quite different in Y cells from those in X cells, and that the Y cells also receive excitatory drive from an additional nonlinear receptive field mechanism.

The nonlinear pathway of Y ganglion cells in the cat retina.

Retinal ganglion cells of the Y type in the cat retina produce two different types of response: linear and nonlinear. The nonlinear responses are generated by a separate and independent nonlinear pathway. The functional connectivity in this pathway is analyzed here by comparing the observed second-order frequency responses of Y cells with predictions of a "sandwich model" in which a static nonlinear stage is sandwiched between two linear filters. The model agrees well with the qualitative and quantitative features of the second-order responses. The prefilter in the model may well be the bipolar cells and the nonlinearity and postfilter in the model are probably associated with amacrine cells.

The eel retina. Ganglion cell classes and spatial mechanisms.

We have been able to separate optic fibers in the eye of the eel Anguilla rostrata into two distinct classes on the basis of spatial summation properties. X fibers, the first class, are like X ganglion cells in the cat: they have null positions for contrast reversal sine gratings; they respond at the modulation frequency; and many have a strong surround mechanism. X fibers, the second class, respond with an "on-off" response to local stimulation, to diffuse light modulation, to coarse drifting gratings, and to contrast reversal gratings. We have put forward a model for the receptive field of X fibers which involves two subunits, with rectification before the subunits add their signals. This model accounts for many of the quirks of X fibers.

The eel retina. Receptor classes and spectral mechanisms.

Light and electron microscopy revealed that there are both rods and cones in the retina of the eel Anguilla rostrata. The rods predominate with a rod to cone ratio of 150:1. The spectral sensitivity of the dark-adapted eyecup ERG had a peak at about 520 nm and was well fit by a vitamin A2 nomogram pigment with a lambdamax = 520 nm. This agrees with the eel photopigment measurements of other investigators. This result implies that a single spectral mechanism--the rods--provides the input for the dark-adapted ERG. The spectral sensitivity of the ERG to flicker in the light-adapted eyecup preparation was shifted to longer wavelengths; it peaked at around 550 nm. However, there was evidence that this technique might not have completely eliminated rod intrusion. Rod responses were abolished in a bleached isolated retina preparation, in which it was shown that there were two classes of cone-like mechanisms, one with lambdamax of 550 nm and the other with lambdamax of less than 450 nm. Ganglion cell recording provided preliminary evidence for opponent-color processing. Horizontal cells were only of the L type with both rod and cone inputs.

The importance of contrast for the activity of single neurons, the VEP and perception.

The brightness of a visually perceived object is mainly determined by the average local contrast around the border between object and background. This fact is demonstrated here with several examples of equiluminant objects on nonuniformly luminant backgrounds. Even in Mondrian-like patterns resembling those used by Land and McCann (1971), equiluminant objects may appear to be of unequal brightness. This result does not agree with predictions of the Retinex Theory. The importance of contrast in vision is also suggested by neurophysiological findings, both classical and recent, that reveal the dependence of visual responses on contrast over most of the visual operating range of mean illumination. The dependence on contrast appears to be the result of retinal gain control mechanisms and is not due to center-surround interaction in the receptive field. We have discovered parallel neural channels with high and low contrast gain in the monkey's visual pathway by means of single unit techniques. Visual evoked potential measurements suggest that similar visual pathways, and with high and low contrast-sensitivity, exist in man and monkey.