M.J.M. Lankheet

Light adaptation in cone vision involves switching between receptor and post-receptor sites

We see over an enormous range of mean light levels, greater than the range of output signals retinal neurons can produce. Even highlights and shadows within a single visual scene can differ ∼10,000-fold in intensity—exceeding the range of distinct neural signals by a factor of ∼100. The effectiveness of daylight vision under these conditions relies on at least two retinal mechanisms that adjust sensitivity in the ∼200 ms intervals between saccades. One mechanism is in the cone photoreceptors (receptor adaptation) and the other is at a previously unknown location within the retinal circuitry that benefits from convergence of signals from multiple cones (post-receptor adaptation). Here we find that post-receptor adaptation occurs as signals are relayed from cone bipolar cells to ganglion cells. Furthermore, we find that the two adaptive mechanisms are essentially mutually exclusive: as light levels increase the main site of adaptation switches from the circuitry to the cones. These findings help explain how human cone vision encodes everyday scenes, and, more generally, how sensory systems handle the challenges posed by a diverse physical environment.

Unraveling adaptation and mutual inhibition in perceptual rivalry.

When the visual system is confronted with incompatible images in the same part of the visual field, the conscious percept switches back and forth between the rivaling stimuli. Such spontaneous flips provide important clues to the neuronal basis for visual awareness. The general idea is that two representations compete for dominance in a process of mutual inhibition, in which adaptation shifts the balance to and fro. The inherent nonlinear nature of the rivalrous flip-flop and its stochastic behavior, however, made it impossible to disentangle inhibition and adaptation. Here we report a general method to measure the time course, and asymmetries, of mechanisms involved in perceptual rivalry. Supported by model simulations, we show the dynamics of opponent interactions between mutual inhibition and adaptation. The findings not only provide new insight into the mechanism underlying rivalry but also offer new opportunities to study and compare a wide range of bistable processes in the brain and their relation to visual awareness.

The spike generating mechanism of cat retinal ganglion cells.

The spike generating mechanism (SGM) of sustained and transient-type ganglion cells has been investigated from intracellular recordings in the cat retina. The relationship between the generator potential and the impulse pattern, which are respectively the input and the output of the SGM, has been studied after separating one component from the other. Comparison of averaged generator potentials and the corresponding PSTHs showed that the spike generator is highly sensitive to changes of the generator potential. It proved to be relatively indifferent to the prevailing average levels of depolarization. During sustained parts of the responses the SGM exhibits a stochastic nature. At higher light flicker frequencies, during spike bursts, on the other hand spike generation is very regular and phase locked to the stimulus. The averaged generator potentials were also used to develop and test a set of minimal, computer simulated models of the spike generator. A slow threshold adaptation (time constant about 50 msec) is absolutely necessary in addition to the faster refractory recovery in order to produce spike patterns similar to those measured during the corresponding response periods. The developed model accounts completely for the observed characteristics of ganglion cell spike generation under a wide variety of light stimulus regimes and both for the sustained and for the transient type of ganglion cell.

The motion reverse correlation (MRC) method: a linear systems approach in the motion domain.

We introduce the motion reverse correlation method (MRC), a novel stimulus paradigm based on a random sequence of motion impulses. The method is tailored to investigate the spatio-temporal dynamics of motion selectivity in cells responding to moving random dot patterns. Effectiveness of the MRC method is illustrated with results obtained from recordings in both anesthetized cats and an awake, fixating macaque monkey. Motion tuning functions are computed by reverse correlating the response of single cells with a rapid sequence of displacements of a random pixel array (RPA). Significant correlations between the cells responses and various aspects of stimulus motion are obtained at high temporal resolution. These correlations provide a detailed description of the temporal dynamics of, for example, direction tuning and velocity tuning. In addition, with a spatial array of independently moving RPAs, the MRC method can be used to measure spatial as well as temporal receptive field properties. We demonstrate that MRC serves as a powerful and time-efficient tool for quantifying receptive field properties of motion selective cells that yields temporal information that cannot be derived from existing methods.

Recovery from adaptation for dynamic and static motion aftereffects: Evidence for two mechanisms

The motion aftereffect (MAE) is an illusory drift of a physically stationary pattern induced by prolonged viewing of a moving pattern. Depending on the nature of the test pattern the MAE can be phenomenally different. This difference in appearance has led to the suggestion that different underlying mechanisms may be responsible and several reports show that this might be the case. Here, we tested whether differences in MAE duration obtained with stationary test patterns and dynamic test patterns can be explained by a single underlying mechanism. We find the results support the existence of (at least) two mechanisms. The two mechanisms show different characteristics: the static MAE (i.e. the MAE tested with a static test pattern) is almost completely stored when the static test is preceded by a dynamic test; in contradistinction, the dynamic MAE is not stored when dynamic testing is preceded by a static test pattern.

Responses of Complex Cells in Area 17 of the Cat to Bi-vectorial Transparent Motion

We examined the responses to transparent motion of complex cells in cat area 17 which show directional selectivity to moving random pixel arrays (RPAs). The response to an RPA moving in the cells preferred direction is inhibited when a second RPA is transparently moving in another direction. The inhibition by the second pattern is quantified as a function of its direction. The response to a pattern moving in the preferred direction is never completely suppressed, not even when a second pattern is moving transparently in the opposite direction. To the extent that supra-spontaneous firing rates signal the presence of the optimal velocity vector, these cells therefore still signal the presence of this line-label stimulus despite additional opposing, or otherwise directed, motion components. The results confirm previous suggestions that, for the computation of motion energy in cat area 17 complex cells, a full opponent stage is not plausible. Furthermore, we show that the response to a combination of two motion vectors can be predicted by the average of the responses to the individual components.

The dynamics of light adaptation in cat horizontal cell responses.

In order to model the dynamic properties of light adaptation processes in cat horizontal (H-) cells, the time course of the gain adjustment following changes in the mean illumination level was studied. H-cell responses were recorded intracellularly in the optically intact, in vivo, eye of the cat. The light stimulus consisted of two spots, a large background spot (8.8 deg diameter) and a concentrically arranged smaller test spot (3.9 deg). The background was either square wave or sine wave modulated in intensity at a frequency of 0.2-1 Hz. The instantaneous value of the response gain was measured with brief flashes (10 msec) of the test spot, generated repetitively at a frequency of 5 or 10 Hz. Modulation of the background intensity, at a contrast of 0.6 and in the photopic range, effectively induces a modulation of the gain. The readjustment of the gain by a stepwise increase or decrease in background illumination is completed within about 200 msec. The amplitude of the gain modulation due to a 0.5 Hz background flicker is quantitatively comparable to that measured between steady illumination levels. Dynamic changes of the gain at low frequency stimuli therefore, have to be taken into account in modelling H-cell responses. For sinusoidal modulations of the background luminance the time course of gain adjustment is quantified by the phase shift of the gain modulation relative to background intensity modulation. The results, together with those described in two preceding papers, are used to test and discuss several light adaptation models that have been proposed previously. It was found that light adaptation in cat H-cells is described more adequately by a de Vries-Rose type of adaptation model than by a Weber type of light adaptation.

Stereoscopic Segregation of Transparent Surfaces and the Effect of Motion Contrast

Stereoscopic segregation in depth was studied using two superimposed frontoparallel surfaces displayed in dynamic random dot stereograms. The two patterns were positioned symmetrically in front of and behind a binocular fixation point. They were either stationary, or they could move relative to each other. Sensitivity for segregation was established by adding gaussian distributed disparity noise to the disparities specifying the two planes, and finding the noise amplitude that gave threshold segregation performance. Observers easily segregate the two surfaces for disparity differences between approximately 6 and 30-40 arcmin. Motion contrast, which by itself provides no cue to perform the task, greatly improves sensitivity for segregation. Noise tolerance rises by a factor of two or more when the patterns move at different speeds, or in different (frontoparallel) directions. The effect increases with directional difference, but the optimal directional difference deviated from 180 deg. The optimal speed varies with disparity difference. Thus, motion and disparity must interact in order to resolve the two transparent planes.

The lateral spread of light adaptation in cat horizontal cell responses

To investigate the sites of light adaptation processes in the mammalian distal retina, we studied the lateral spread of adaptation signals in cone-driven cat horizontal (H-) cell responses. The size of the adaptation pool is compared to the receptive field for H-cell responses. H-cell activity was recorded intracellularly in the optically intact, in vivo eye. It is demonstrated that light adaptation as measured in H-cells is not a strictly local process. Background light falling outside a central test region effectively modulates the responses to a small test light, flashed on the receptive field center. The integration area for adaptation signals was quantitatively compared to the H-cell receptive field size by measuring the desensitizing effect of background light on the responses to a small centered test spot, as a function of background spot size. The area-adaptation function is comparable to the area-response function but has a slightly smaller length constant. Light adaptation in H-cell responses, therefore, reveals spread of adaptation over a large distance and is probably mediated through lateral interactions in the H-cell network rather than in the cones.

Light adaptation and frequency transfer properties of cat horizontal cells.

The frequency transfer properties of horizontal cells in the cat retina were studied as a function of the mean light intensity level and stimulus contrast. To this end, horizontal cell responses to sinusoidally modulated light stimuli were recorded intracellularly in the optically intact, in vivo eye. The light stimulus consisted of a 3.9 deg dia. spot superimposed on a steady background (8.8 deg dia.). A discrete Fourier analysis was performed in order to describe the amplitude and phase characteristics of the linear response component and in order to specify the nonlinear distortion of the response. The amplitude of the fundamental Fourier component was found to increase linearly with the contrast of the sinusoidal light intensity modulation. Increasing the mean light level while keeping the contrast constant caused a frequency dependent increase in response amplitude. The increase was most pronounced at high temporal frequencies and resulted in a conspicuous increase of the flicker fusion frequency. Steady background illumination caused a reduction of the response amplitudes at the lower temporal frequencies. Responses in the high frequency range, however, were not affected. The phase shifts of the fundamental Fourier components were found to diminish at increasing mean illumination levels. The harmonic distortion of horizontal cell responses to sinewave flicker was studied as a function of stimulus frequency and stimulus contrast. By comparing the data obtained using sinusoidal light intensity modulation with the intensity profiles described in a preceding paper it was investigated to what extent the harmonic distortion can be explained by the nonlinearity expressed in the response vs intensity profiles.