Moshe Gur

Response Variability of Neurons in Primary Visual Cortex (V1) of Alert Monkeys

Response variability of neurons limits the reliability and resolution of sensory systems. It is generally thought that response variability in the visual system increases at cortical levels, but the causes of the variability have not been identified. We have measured the response variability of neurons in primary visual cortex (V1) of alert monkeys. We recorded from 80 single cells distributed over all V1 layers and from 8 parvocellular cells of the lateral geniculate nucleus. All cells were stimulated with a bar of near-optimal orientation, color, and dimensions while continuously monitoring the eye movements of fixation. To minimize the effects of eye movements, responses that occurred while the eye was relatively steady were selected for analysis. The impulses elicited by each stimulus presentation were counted, and the variance and coefficient of variation were computed. Both measures of response variability were much lower than reported previously for V1 cells of both alert and anesthetized monkeys. Our data show that fixational eye movements cause a large component of response variance in alert monkeys. Moreover, the reliability of V1 neurons is not obviously degraded compared with lateral geniculate nucleus cells. The high reliability of neurons in alert monkeys is consistent with expectations from conventional biophysical models, and it suggests that activity in a modest number of neurons may suffice to form a perceptual decision.

A dissociation between brain activity and perception: chromatically opponent cortical neurons signal chromatic flicker that is not perceived.

When two isoluminant colors alternate at frequencies > 10 Hz, we perceive only one fused color with a minimal sensation of brightness flicker. In spite of the perception of color fusion, color opponent (CO) cells at early stages of the visual pathway are known to respond to chromatic flicker at frequencies far exceeding the perceptual fusion frequency. To explain color fusion, several groups have predicted that CO cells in V1-unlike the retina and lateral geniculate nucleus-should not follow high-frequency flicker. To test this prediction we recorded from 12 CO cells in various V1 layers. We found, contrary to expectations, that these neurons follow high frequency flicker well above heterochromatic fusion frequencies. All followed 15 Hz flicker and 10/12 followed 30 Hz flicker. For three cells, we tested 60 Hz luminance flicker and found clear responses. We thus present evidence of cortical activity in alert, trained monkeys that is clearly representing visual stimulation, yet is not perceived. Our data call into question explanations of perceptual phenomena that invoke a low temporal frequency cut-off of CO cells in V1 to account for the failure to perceive fast temporal changes in the chromatic domain.

Selective activation of visual cortex neurons by fixational eye movements: implications for neural coding.

During normal vision, when subjects attempt to fix their gaze on a small stimulus feature, small fixational eye movements persist. We have recorded the impulse activity of single neurons in primary visual cortex (V1) of macaque monkeys while their fixational eye movements moved the receptive-field activating region (AR) over and around a stationary stimulus. Three types of eye movement activation were found. (1) Saccade cells discharged when a fixational saccade moved the AR onto the stimulus, off the stimulus, or across the stimulus. (2) Position/drift cells discharged during the intersaccadic (drift) intervals and were not activated by saccades that swept the AR across the stimulus without remaining on it. To activate these neurons, it was essential that the AR be placed on the stimulus and many of these cells were selective for the sign of contrast. They had smaller ARs than the other cell types. (3) Mixed cells fired bursts of activity immediately following saccades and continued to fire at a lower rate during intersaccadic intervals. The tendency of each neuron to fire transient bursts or sustained trains of impulses following saccades was strongly correlated with the transiency of its response to stationary flashed stimuli. For one monkey, an extraretinal influence accompanying fixational saccades was identified. During natural viewing, the different eye movement classes probably make different contributions to visual processing. Position/drift neurons are well suited for coding spatial details of the visual scene because of their small AR size and their selectivity for sign of contrast and retinal position. However, saccade neurons transmit information that is ambiguous with respect to the spatial details of the retinal image because they are activated whether the AR lands on a stimulus contour, or the AR leaves or crosses the contour and lands in another location. Saccade neurons may be involved in constructing a stable world in spite of incessant retinal image motion, as well as in suppressing potentially confusing input associated with saccades.

Saccades and drifts differentially modulate neuronal activity in V1: Effects of retinal image motion, position, and extraretinal influences

In natural vision, continuously changing input is generated by fast saccadic eye movements and slow drifts. We analyzed effects of fixational saccades, voluntary saccades, and drifts on the activity of macaque V1 neurons. Effects of fixational saccades and small voluntary saccades were equivalent. In the presence of a near-optimal stimulus, separate populations of neurons fired transient bursts after saccades, sustained discharges during drifts, or both. Strength, time course, and selectivity of activation by fast and slow eye movements were strongly correlated with responses to flashed or to externally moved stimuli. These neuronal properties support complementary functions for post-saccadic bursts and drift responses. Local post-saccadic bursts signal rapid motion or abrupt change of potentially salient stimuli within the receptive field; widespread synchronized bursts signal occurrence of a saccade. Sustained firing during drifts conveys more specific information about location and contrast of small spatial features that contribute to perception of fine detail. In addition to stimulus-driven responses, biphasic extraretinal modulation accompanying saccades was identified in one third of the cells. Brief perisaccadic suppression was followed by stronger and longer-lasting enhancement that could bias perception in favor of saccade targets. These diverse patterns of neuronal activation underlie the dynamic encoding of our visual world.

Visual stability and space perception in monocular vision: mathematical model

A deterministic model for monocular space perception is presented. According to the model, retinal luminance changes due to involuntary eye movements are detected and locally analyzed to yield the angular velocity of each image point. The stable three-dimensional spatial coordinates of viewed objects are then reconstructed using a method of infinitesimal transformations. The extraction of the movement (parallax) field from the optical flow is represented by a set of differential equations, the derivation of which is based on the conservation of energy principle. The relation of the model to retinal neurophysiology and to various aspects of visual space perception is discussed.

Visual receptive fields of neurons in primary visual cortex (V1) move in space with the eye movements of fixation.

We tested the hypothesis that receptive field (RF) locations of visual cortex cells maintain a fixed location on the retina and move in space with movements of the eye. Responses to a bar swept across the RF were recorded from 29 neurons in V1 (26) and V2 (3) of alert monkeys while precisely monitoring the eye movements of fixation. There was a tight correlation and a near unity ratio between eye position and RF position. This implies that RFs of V1 neurons and at least some V2 neurons are fixed to specific retinal locations, rather than being shifted on the retina by attention-controlled mechanisms. V1 neurons thus differ from those polysensory neurons whose RF locations on the retina are dynamically altered to maintain a desired position in space.

Isoluminant stimuli may not expose the full contribution of color to visual functioning: Spatial contrast sensitivity measurements indicate interaction between color and luminance processing

Visual performance is greatly impaired when tested with heterochromatic isoluminant stimuli. It is thus concluded that the chromatic system contribution to many visual tasks is limited. We suggest that unless color and luminance are shown to be processed independently, such experiments do not demonstrate shortcomings of the chromatic system but rather the inadequacy of using isoluminant stimuli for isolating that system. We hypothesize that color vision has evolved not only to encode color per se but also to enhance luminance-based visual processing, so that for color information to be fully effective, luminance as well as chromatic variations should be present in the stimulus. The hypothesis was tested by studying the contribution of color to spatial vision. The human contrast sensitivity function (CSF) was studied using luminance, isoluminance (color) and combined luminance/color sinusoidal gratings. It is found that luminance contrast sensitivity is enhanced when luminance contrast is accompanied by color contrast and vice versa. The nature of the interaction is best described by an additive single analyzer model. Color opponent cells which respond to both chromatic and achromatic stimuli may be identified as the analyzer.

Studying striate cortex neurons in behaving monkeys: benefits of image stabilization.

Responses of single cells in the striate cortex of a behaving monkey were studied while the eye movements of fixation were monitored with high precision. Receptive fields of cortical neurons moved in space with the eye. When the eye position signal was used to stabilize the image on the retina, response rates were more vigorous and more reliable. When the image was not stabilized, the estimates of receptive field activating areas were influenced (usually inflated) in unpredictable ways. With stabilization, small receptive fields can be studied and powerful surround interactions become apparent.

Frequency-domain analysis of the human electroretinogram

Normal corneal electroretinograms (ERG) are analyzed in the frequency domain using the fast Fourier transform (FFT) and linear prediction (LP) methods. Four dominant frequencies at 18, 79, 126, and 159 Hz are found in the dark-adapted state. Light adaptation shifts the low frequency to higher frequency and the mid- and the two high-frequency components to lower frequencies. The relative amplitude of the high-frequency component resulting from the oscillatory potentials is quantified. It is shown that frequency-domain features are of a smaller variability than time-domain components, and can be extracted even from a noisy surface ERG.

Direction selectivity in V1 of alert monkeys: evidence for parallel pathways for motion processing

In primary visual cortex (V1) of macaque monkeys, motion selective cells form three parallel pathways. Two sets of direction selective cells, one in layer 4B, and the other in layer 6, send parallel direct outputs to area MT in the dorsal cortical stream. We show that these two outputs carry different types of spatial information. Direction selective cells in layer 4B have smaller receptive fields than those in layer 6, and layer 4B cells are more selective for orientation. We present evidence for a third direction selective pathway that flows through V1 layers 4Cm (the middle tier of layer 4C) to layer 3. Cells in layer 3 are very selective for orientation, have the smallest receptive fields in V1, and send direct outputs to area V2. Layer 3 neurons are well suited to contribute to detection and recognition of small objects by the ventral cortical stream, as well as to sense subtle motions within objects, such as changes in facial expressions.