Visual cortical neurons: are bars or gratings the optimal stimuli?

Neurons in the visual cortex of monkeys and cats have been characterized as either (i) bar and edge detectors or (ii) cells selective for certain spatial frequencies. To assess which of these functional descriptions is more accurate, we measured (i) the selectivity and (ii) the responsivity-sensitivity of these neurons to bars of various widths and gratings of various spatial frequencies. All of the cells recorded from were considerably more selective along the dimension of spatial frequency than along the dimension of bar width. Further, most were more responsive and sensitive to the grating of optimal frequency than to the bar of optimal width.

Maintaining the cornea and the general physiological environment in visual neurophysiology experiments.

Neurophysiologists have been investigating the responses of neurons in the visual system for the past half-century using monkeys and cats that are anesthetized and paralyzed, with the non-blinking eyelids open for prolonged periods of time. Impermeable plastic contact lenses have been used to prevent dehydration of the corneal epithelium, which would otherwise occur in minutes. Unfortunately, such lenses rapidly introduce a variety of abnormal states that lead to clouding of the cornea, degradation of the retinal image, and premature termination of the experiment. To extend the viability of such preparations, a new protocol for maintenance of corneal health has been developed. The protocol uses rigid gas permeable contact lenses designed to maximize gas transmission, rigorous sterile methods, and a variety of methods for sustaining and monitoring the overall physiology of the animal. The effectiveness of the protocol was evaluated clinically by ophthalmoscopy before, during, and after the experiments, which lasted 8-10 days. Histopathology and quantitative histology were performed on the corneas following the experiment. Our observations showed that this protocol permits continuous contact lens wear without adversely affecting the corneas. Thus, it is possible to collect data 24 h each day, for the entire duration of the experiment.

Bayesian analysis of identification performance in monkey visual cortex: nonlinear mechanisms and stimulus certainty.

The identification performance of single neurons in the primary visual cortex was quantified by measuring how accurately one could know the stimulus based upon the neuron's response. We found that for a typical neuron a response of 10 action potentials, following one brief stimulus presentation, was sufficient to classify the stimulus as belonging to a relatively small region in stimulus space, with a high degree of confidence. The performance was better than that which could be attained through linear summation of excitation and inhibition alone. The results suggest that the enhanced performance is a consequence of two nonlinear mechanisms: contrast gain control and expansive response exponent.

Cortical neurons: isolation of contrast gain control.

The selectivity of cortical neurons remains invariant with contrast, even though the contrast-response function saturates. Both the invariance and the saturation might be due to a contrast-gain control mechanism. To test this hypothesis, a drifting grafting was used to measure the contrast-response function, while a counterphase grating was simultaneously presented at the null position of the receptive field (where it evokes no response at any contrast). When the contrast of the counterphase grating increased, the contrast-response function shifted primarily to the right. This result is consistent with the hypothesis that there is a fast-acting gain-control mechanism which effectively scales the input contrast by the average local contrast.

Spatial frequency selectivity of cells in macaque visual cortex.

We measured the spatial frequency contrast sensitivity of cells in the primate striate cortex at two different eccentricities to provide quantitative statistics from a large population of cells. Distributions of the peak frequencies and bandwidths are presented and examined in relationship to (a) each other, (b) absolute contrast sensitivity, (c) orientation tuning, (d)retinal eccentricity, and (e) cell type. Simple and complex cells are examined in relationship to linear/nonlinear (that is, X/Y) properties; a procedure is described which provides a simple, reliable and quantitative method for classifying and describing striate cells. Among other things, it is shown that (a) many stirate cells have quite narrow spatial bandwidths and (b) at a given retinal eccentricity, the distribution of peak frequency covers a wide range of frequencies; these findings support the basic multiple channel notion. The orientation tuning and spatial frequency tuning which occurs at the level of striate cortex (in a positively correlated fashion) suggests that the cells might best be considered as two-dimensional spatial filters.

Visual cortical receptive fields in monkey and cat: spatial and temporal phase transfer function.

The response amplitude of simple cortical cells to spatiotemporal sine-wave patterns has been thoroughly documented in both cat and monkey. However, comparable measurements of response phase are not available even though phase measurements are essential for estimating the complete transfer function of a cell, and thus its spatiotemporal receptive field. This report describes a simple procedure for measuring both the amplitude and the phase transfer functions of striate cells. This technique was applied to 15 monkey and 27 cat simple cells. The spatiotemporal phase response functions were found to be adequately described by linear equations in four parameters. Both the amplitude and phase responses were found to satisfy several strong constraints implied by the class of linear quadrature models proposed recently in theories of biological motion sensitivity. Because the data satisfied these constraints, it was possible to determine four important receptive field properties from the phase data: the spatial symmetry, the temporal symmetry, the response latency, and the spatial position. The receptive fields were found to have a wide range of spatial symmetries, but a more narrow range of temporal symmetries. Spatiotemporal receptive fields reconstructed from complete transfer functions are used to illustrate some of the differences between direction selective and nondirection selective cells. Finally, the effects of linear and nonlinear mechanisms on amplitude, phase, and direction selective responses are considered.

Spatial mapping of monkey V1 cells with pure color and luminance stimuli.

We recorded the responses of single macaque striate cortical cells to color-varying and luminance-varying patterns. We show that (a) the vast majority of primate striate cells respond to pure color stimuli, in addition to responding to luminance-varying stimuli (b) in general, simple cells are color-selective whereas complex cells respond to multiple color regions, (c) most cortical cells show bandpass spatial frequency tuning to pure color-varying gratings, with various cells tuned to each of a wide range of spatial frequencies and (d) the peak spatial frequency and bandwidth of most striate cells is the same for color as for luminance-varying gratings; when they differ, cells tend to be more broadly tuned and peak at lower spatial frequencies for color (e) complex cells, on the average, respond to higher spatial frequencies than do simple cells.

Classifying simple and complex cells on the basis of response modulation.

Hubel and Wiesel (1962; Journal of Physiology, London, 160, 106-154) introduced the classification of cortical neurons as simple and complex on the basis of four tests of their receptive field structure. These tests are partly subjective and no one of them unequivocally places neurons into distinct classes. A simple, objective classification criterion based on the form of the response to drifting sinusoidal gratings has been used by several laboratories, although it has been criticized by others. We review published and unpublished evidence which indicates that this simple and objective criterion reliability divides neurons of the striate cortex in both cats and monkeys into two groups that correspond closely to the classically-described simple and complex classes.

Visual cortex neurons in monkey and cat: effect of contrast on the spatial and temporal phase transfer functions.

The responses of simple cells (recorded from within the striate visual cortex) were measured as a function of the contrast and the frequency of sine-wave grating patterns in order to explore the effect of contrast on the spatial and temporal phase transfer functions and on the spatiotemporal receptive field. In general, as the contrast increased, the phase of the response advanced by approximately 45 ms (approximately one-quarter of a cycle for frequencies near 5 Hz), although the exact value varied from cell to cell. The dynamics of this phase-advance were similar to the dynamics of the amplitude: the amplitude and the phase increased in an accelerating fashion at lower contrasts and then saturated at higher contrasts. Further, the gain for both the amplitude and the phase appeared to be governed by the magnitude of the contrast rather than the magnitude of the response. For the spatial phase transfer function, variations in contrast had little or no systematic effect; all of the phase responses clustered around a single straight line, with a common slope and intercept. This implies that the phase-advance was not due to a change in the spatial properties of the neuron; it also implies that the phase-advance was not systematically related to the magnitude of the response amplitude. On the other hand, for the temporal phase transfer function, the phase responses fell on five straight lines, related to the five steps in contrast. As the contrast increased, the phase responses advanced such that both the slope and the intercept were affected. This implies that the phase-advance was a result of contrast-induced changes in both the response latency and the shape/symmetry of the temporal receptive field.

Motion selectivity and the contrast-response function of simple cells in the visual cortex.

The responses of simple cells were recorded from the visual cortex of cats, as a function of the position and contrast of counterphase and drifting grating patterns, to assess whether direction selectivity can be accounted for on the basis of linear summation. The expected responses to a counterphase grating, given a strictly linear model, would be the sum of the responses to the two drifting components. The measured responses were not consistent with the linear prediction. For example, nearly all cells showed two positions where the responses approached zero (i.e. two "null phase positions"); this was true, even for the most direction selective cells. However, the measured responses were consistent with the hypothesis that direction selectivity is a consequence of the linear spatiotemporal receptive-field structure, coupled with the nonlinearities revealed by the contrast-response function: contrast gain control, halfwave rectification, and expansive exponent. When arranged in a particular sequence, each of these linear and nonlinear mechanisms performs a useful function in a general model of simple cells. The linear spatiotemporal receptive field initiates stimulus selectivity (for direction, orientation, spatial frequency, etc.). The expansive response exponent enhances selectivity. The contrast-set gain control maintains selectivity (over a wide range of contrasts, in spite of the limited dynamic response range and steep slope of the contrast-response function). Rectification conserves metabolic energy.

Visual cortex neurons in monkeys and cats: detection, discrimination, and identification.

A descriptive function method was used to measure the detection, discrimination, and identification performance of a large population of single neurons recorded from within the primary visual cortex of the monkey and the cat, along six stimulus dimensions: contrast, spatial position, orientation, spatial frequency, temporal frequency, and direction of motion. First, the responses of single neurons were measured along each stimulus dimension, using analysis intervals comparable to a normal fixation interval (200 ms). Second, the measured responses of each neuron were fitted with simple descriptive functions, containing a few free parameters, for each stimulus dimension. These functions were found to account for approximately 90% of the variance in the measured response means and response standard deviations. (A detailed analysis of the relationship between the mean and the variance showed that the variance is proportional to the mean.) Third, the parameters of the best-fitting descriptive functions were utilized in conjunction with Bayesian (optimal) decision theory to determine the detection, discrimination, and identification performance for each neuron, along each stimulus dimension. For some of the cells in monkey, discrimination performance was comparable to behavioral performance; for most of the cells in cat, discrimination performance was better than behavioral performance. The behavioral contrast and spatial-frequency discrimination functions were similar in shape to the envelope of the most sensitive cells; they were also similar to the discrimination functions obtained by optimal pooling of the entire population of cells. The statistics which summarize the parameters of the descriptive functions were used to estimate the response of the visual cortex as a whole to a complex natural image. The analysis suggests that individual cortical neurons can reliably signal precise information about the location, size, and orientation of local image features.

Striate cortex responses to periodic patterns with and without the fundamental harmonics.

1. The visual system has been modelled as a set of independent linear channels each tuned to a limited band of spatial frequency with the average bandwidth being approximately 1 octave. A great deal of psychophysical and physiological evidence supports this basic notion. However, Henning, Hertz & Broadbent (1975) have shown reciprocal masking between a fundamental frequency (1F) and a complex grating composed of higher harmonics several octaves removed ((4+5+6)F); their results clearly indicate a lack of independence.2. We recorded the activity of cells in the striate cortex of monkeys and cats using stimuli similar to those of Henning et al. to make comparisons with their psychophysical data and to test specific physiological predictions.3. We found that cells tuned to the fundamental frequency did not produce an excitatory response to the (4+5+6)F pattern. However, the response of such cells to 1F could be reduced by simultaneous presentation of (4+5+6)F. Similarly, the response of cells tuned to high frequencies, when presented with (4+5+6)F, was reduced by simultaneous presentation of 1F. However, this reciprocal inhibition could be produced between single harmonics (e.g. 1F and 4F) and was not dependent upon a special relationship between 1F and (4+5+6)F.4. When cells tuned to high frequencies were presented with the (4+5+6)F pattern they generated predictable responses in the higher harmonics (4, 5, 6) but they also generated an unexpected, non-linear, response at the fundamental frequency, 1F, even though no such low frequency component was present in the stimulus. This effect is due to the response rectification which striate cells show.5. In support of the linear independent spatial frequency channel model, we find (a) striate cells provide an excitatory response to only a limited range of frequencies, (b) they do not provide such responses to the ;apparent' yet ;missing' fundamental in the (4+5+6)F beating pattern, and (c) the response wave form to complex stimuli like (4+5+6)F is reasonably predictable (at least for simple cells) from the model. Against the model we find that (a) frequencies outside the excitatory bandpass can produce inhibition and (b) the rectification of the response wave form introduces harmonics not present in the stimulus.

Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex.

Spatial contrast adaptation, produced by prolonged exposure to high contrast grating patterns, has become an important psychophysical method for isolating spatial and orientation selective channels in the human visual system. It has been reasonably argued that this adaptation may be fundamentally dependent upon the activity of neurones in the striate cortex. To test the validity of this hypothesis, and several others, we measured the general adaptation characteristics of 144 striate neurones using a stimulus protocol comparable to the typical psychophysical methods. In general, during prolonged high contrast stimulation, the responses of most cells exponentially decayed from a transient peak response to a sustained plateau response; following adaptation, the responses to lower contrasts were depressed relative to the unadapted state but then gradually recovered from the transient depression to a sustained plateau. Such adaptation was a property common to both simple and complex cells (the distributions of the quantitative of adaptation were overlapping); there were however small but reliable differences. We compared the neurophysiological contrast adaptation with two psychophysical estimates of human contrast adaptation (threshold contrast elevation and apparent contrast reduction) and found that the time courses and the magnitudes were quite similar. The effect of contrast adaptation on the spatial frequency tuning was assessed by measuring the contrast response function at several different test spatial frequencies before and after adaptation at the optimum centre frequency. We found that the effect of adaptation decreased as the difference between test and adaptation frequency increased. Grating contrast adaptation has been alternatively described as 'constructive gain control' on the one hand and as 'deleterious fatigue' on the other. We tested the effect of contrast adaptation on the contrast response function and found (a) that adaptation shifts the curves vertically downward parallel to the response axis (thus reflecting a decrease in the maximum rate of firing and a deleterious compression of the response range) and (b) that adaptation shifts the curves horizontally to the right parallel to the contrast axis (thus reflecting a true sensitivity shift of the remaining response range for constructive maintenance of high differential sensitivity around the prevailing background level).(ABSTRACT TRUNCATED AT 400 WORDS)

Discrimination performance of single neurons: rate and temporal-pattern information.

1. A new method of measuring the performance of neurons in sensory discrimination tasks was developed and then applied to single-neuron responses recorded in the auditory nerve of chinchilla and in the striate visual cortex of cat. 2. Most previous methods of measuring discrimination performance have employed decision rules that involve comparing the total counts of action potentials (spikes) produced by two different stimuli. Such measures ignore response pattern and hence may not reflect all the information transmitted by a neuron. The proposed method attempts to measure all (or most) of the transmitted information by constructing descriptive models of the neuron's response to each stimulus in the discrimination experiment; these descriptive models consist of measured probability distributions of the spike counts in small time bins. The measured probability distributions are then used to define an optimal decision rule (an ideal observer) for discriminating the two stimuli. Finally, discrimination performance is measured by applying this decision rule to novel presentations of the same two stimuli. 3. Intensity and temporal-phase discrimination were measured for three neurons in the auditory nerve of chinchilla. The discrimination stimuli were low-frequency pure tones of 70-ms duration. Intensity thresholds were found to be 5-20 dB lower at low intensities using the new pattern method compared with the traditional counting method. The pattern method led to better performance because it utilized both rate and temporal pattern information. Phase discrimination performance using the counting method was at chance because the average spike rate did not change with phase. On the other hand, using the pattern method, phase discrimination thresholds were found to decrease with intensity, often reaching values equivalent to 30-40 microseconds of temporal offset. These thresholds are as good as or better than behavioral thresholds in chinchilla. 4. Contrast and temporal-phase discrimination were measured for three neurons in the striate visual cortex of cat. The discrimination stimuli were drifting sine-wave gratings of 100- to 160-ms duration. Contrast discrimination functions measured by the pattern method and the counting method were found to be essentially identical. Phase discrimination using the counting method was at chance. However, using the pattern method, phase thresholds were found to decrease with contrast, reaching values equivalent to 7 ms of temporal offset for the two simple cells. 5. Our results suggest that temporal response pattern carries substantial information for intensity and phase discrimination in the auditory nerve and for phase discrimination in the striate visual cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Motion direction signals in the primary visual cortex of cat and monkey.

When an image feature moves with sufficient speed it should become smeared across space, due to temporal integration in the visual system, effectively creating a spatial motion pattern that is oriented in the direction of the motion. Recent psychophysical evidence shows that such "motion streak signals" exist in the human visual system. In this study, we report neurophysiological evidence that these motion streak signals also exist in the primary visual cortex of cat and monkey. Single neuron responses were recorded for two kinds of moving stimuli: single spots presented at different velocities and drifting plaid patterns presented at different spatial and temporal frequencies. Measurements were made for motion perpendicular to the spatial orientation of the receptive field ("perpendicular motion") and for motion parallel to the spatial orientation of the receptive field ("parallel motion"). For moving spot stimuli, as the speed increases, the ratio of the responses to parallel versus perpendicular motion increases, and above some critical speed, the response to parallel motion exceeds the response to perpendicular motion. For moving plaid patterns, the average temporal tuning function is approximately the same for both parallel motion and perpendicular motion; in contrast, the spatial tuning function is quite different for parallel motion and perpendicular motion (band pass for the former and low pass for the latter). In general, the responses to spots and plaids are consistent with the conventional model of cortical neurons with one rather surprising exception: Many cortical neurons appear to be direction selective for parallel motion. We propose a simple explanation for "parallel motion direction selectivity" and discuss its implications for the motion streak hypothesis. Taken as a whole, we find that the measured response properties of cortical neurons to moving spot and plaid patterns agree with the recent psychophysics and support the hypothesis that motion streak signals are present in V1.

Periodicity of striate-cortex-cell receptive fields.

If striate cells had the simple bipartite or tripartite receptive fields (RF's) classically attributed to them, they should be quite broadly tuned for spatial frequency. Most striate-cortex cells, however, are fairly narrowly tuned and would be expected to have more-periodic RF's. We have examined this question in recordings of the responses of cat and monkey striate-cortex cells to gratings of increasingly large number of cycles, all centered on the cells' RF's. Simple cells narrowly tuned for spatial frequency were found to increase their responses with increasing numbers of stimulus cycles beyond the 1 1/2 cycles expected from the classical RF shape. Broadly tuned simple cells were found to have less-periodic RF's. Whereas narrowly tuned complex cells were also found to respond maximally to many stimulus cycles, other more broadly tuned complex cells did as well (possibly reflecting summation across many broadly tuned simple cells without regard to phase). A suppressive region was often seen just outside the excitatory two-dimensional spatial-frequency region, at off orientations and/or off spatial frequencies and around the whole RF in space. Most striate cells can thus be described as having periodic RF's in the space domain such that they fire just to patterns whose local spatial-frequency spectra fall within a compact, restricted, roughly circular two-dimensional spatial-frequency region, with an encircling suppressive region in both the space and the frequency domains.