Simple cells in cat striate cortex: responses to stationary flashing and to moving light bars

Summary Cells in the simple family respond to a moving light bar with an average response histogram that is most commonly unimodal (single peak: encounter frequency, 64%) and less commonly bimodal (33%) or trimodal (3%). The mean width of the principal response peak given by hypercomplex I cells is narrower than that of simple cells and they have a lower mean optimal stimulus velocity. In a series of 74 cells (simple, 47; hypercomplex I, 27), detailed comparison of the spatial relations between the response peaks to the moving bar and the subregions to the stationary flashing bar led to the concept of a boundary response. The term boundary response refers to an isolated response peak occurring as a moving light bar leaves an OFF subregion that is the last in the sequence of subregions traversed by the bar. The presence of a boundary response leads to an apparent discrepancy between the number of response peaks to a moving light bar and the number of ON subregions in the static-field plot. The boundary response is necessarily completely direction selective. A detailed comparison of the properties of cells as revealed by hand and quantitative methods showed a very good agreement between the two methods in respect to the assignment of cells to the simple, B- and complex cell families. There were, however, serious discrepancies in respect to the receptive field organization of cells in the simple family. In particular, many cells that either failed to respond adequately to hand stimulation by a stationary flashing bar or exhibited only a single receptive field subregion, all responded with two or more subregions when examined quantitatively by the same kind of stationary stimulus.     

Direction selectivity of simple cells in cat striate cortex to moving light bars

Summary Quantitative estimates of the direction selectivities of 118 simple cells in response to moving light bars were expressed as a percentage calculated from the ratio of the response peaks: (preferred minus nonpreferred)/preferred. Virtually all simple cells were direction selective to some degree (mean direction selectivity 73.6%). Static-field plots to a stationary flashing bar were prepared from 74 of the 118 cells. Particular attention was given to the 42 cells with only two subregions in their static-field plot, one subregion responding at light on and the other at light off. It was concluded that interactive effects between subregions, whether synergistic or antagonistic, have little if any influence on the direction selective mechanism when the stimulus is a narrow light bar. Eighty two of the 118 cells were also tested with moving light and dark edges and of these 53 had response profiles with only two response peaks, one to the light edge and the other to the dark edge. Forty one of the 53 cells were each not only direction selective for both a light edge and a dark edge but also had a preferred direction for both edges that was the same as that for a light bar. Only two cells had preferred directions for both light and dark edges that were opposite to the direction preferred by the light bar. With one possible exception, every cell with two response peaks to moving edges and two subregions in the static-field plot showed a one-to-one correspondence between the ordinal sequence of the response peaks and the ordinal sequence of the subregions. Depending upon the polarity of the moving edge and the ordinal sequence of the subregions, the mean level of the direction selectivity to a moving edge was significantly below that to a narrow moving light bar. This reduction in the degree of the direction selectivity appears to be due to an interaction between the subregions leading to a reduction in the amplitude of the response in the preferred direction rather than a suppression of the direction selective mechanism that operates in the nonpreferred direction. Moving edges cause a weak interactive effect between the subregions that seems always to reduce the degree of the direction selectivity, never increasing it.     

Spatial summation of responses in receptive fields of single cells in cat striate cortex

Summary Spatial summation of responses in striate neurons in cats under N₂O/O₂ anaesthesia was examined quantitatively both along the line of the optimal stimulus orientation (length summation) using moving light bars and single light and dark edge stimuli, and at right angles to the optimal orientation (width summation) using stationary flashing bars. Activity profiles and length-response curves were prepared from simple, complex and hypercomplex I and II cells. An activity profile indicates the responsiveness of a cell at locations along the length of its receptive field. The activity profiles from all cell types were usually well fitted by Gaussian functions. Length summation occurs both in end-free (simple and complex) and, to a lesser extent, in end-stopped (hypercomplex I and II) cells over a wide range of stimulus contrasts (0.13 to 0.95). The linearity of length summation was tested either by comparing the recorded length-response curves with the curves predicted from the linear integration of the activity profiles or by comparing the response to the activation of two regions of the receptive field with the sum of the responses to each region activated separately. Although length summation was usually non-linear (either greater than or less than direct proportionality) it was more nearly linear in complex than it was in simple and hypercomplex I cells. Mechanisms responsible for non-linear length summation were studied, including a threshold for discharge, response saturation and summation of end-zone inhibition. Complex cells show little width summation for bars wider than 0.3 °. In simple and hypercomplex I cells there was also relatively little width summation either in an ON or an OFF discharge region at contrasts above about 0.4 but at lower contrasts width summation may be approximately linear. Spatial summation of responses does not appear to be a useful characteristic for distinguishing one striate cell type from another.     

Spatial arrangements of responses by cells in the cat visual cortex to light and dark bars and edges

Summary Detailed examination is made of the responses of visual cortical cells (area 17, border 17–18 and adjacent area 18) in the anaesthetized cat to stationary flashing bars and to bars (lines) and edges moving at their optimal velocities. Particular attention is given to the receptive field organization of cells in the simple family. While there is good general agreement between the main receptive field subregions revealed by stationary and moving stimuli, the responses to moving light and dark bars, supplemented by the responses to moving light and dark edges, provide a much more rapid, accurate and complete guide to the spatial organization of the receptive fields than do the response profiles to a stationary flashing bar. Moving light and dark bars between them generally reveal more subregions in the receptive fields of simple cells than is evident from the response profiles to a stationary flashing bar, particularly when the receptive fields have many subregions. In addition the responses to moving edges provide a rapid guide to spatial summation across the width of a subregion and the possible antagonistic effects of the next subregion in sequence.Two subclasses of cells in the simple family have been recognized: ordinary simple and fast simple cells. Two cell classes (A-cells and silent periodic cells) having properties intermediate between simple and complex types are discriminated and their properties described.     

Binocular interaction on single units in cat striate cortex: Simultaneous stimulation by single moving slit with receptive fields in correspondence

Summary Averaged responses of binocularly-activated single units of the striate cortex of paralysed cats were studied using a single, moving visual stimulus and prisms of variable power to control the visual direction of each eye. Binocular facilitation, summation or occlusion of the monocular response occurred, depending on the type of unit and on the prism setting. Binocular stimulating conditions were optimal for a given unit when the prism setting superimposed, or very nearly superimposed, the receptive field pair on the same plane as the moving stimulus. Under these optimal conditions, most units showed summation or facilitation of the monocular responses, with a minority showing occlusion. When the prism setting was changed from the optimal value, binocular occlusion could be demonstrated in all units.Curves plotting binocular response against prism setting provided information on the specificity, temporal properties and symmetry of the binocular response. The binocular response of simple units showed great specificity with a sharply defined peak on the response curve at a particular prism setting. There was variation from one simple unit to another in the exact prism setting required to give the optimal response. A proportion of complex units, despite large receptive field size, showed binocular specificity with a very narrow range of facilitation, of the same order as that shown by simple units. Other complex units showed binocular facilitation over a wide range of prism settings.Selby Fellow of the Australian Academy of Sciences.     

Receptive field organization of simple cells in cat striate cortex

Summary The receptive field organization of simple cells was studied by analyzing interaction effects between two stationary flashing light stimuli. One stimulus was positioned in the most responsive part of the receptive field to produce activity against which the effects of the other stimulus in various positions of the visual field could be determined.The receptive field was subdivided into an elongated center and elongated antagonistic flanks. The effects on the flanks were always considerably stronger on one side. Powerful flank suppression could be elicited within a region which usually was only slightly wider than the receptive field center. The suppression was just as stimulus specific as the activation of the center and occurred only by light ON or OFF. The cells were classified into ON-dominant and OFF-dominant depending on the kind of response found in the center. In ON-dominant cells the strong flank suppression occurred only by light ON, and light OFF produced enhancement. Correspondingly, the strong flank suppression occurred only by light OFF in OFF-dominant cells.This is consistent with the interpretation that simple cells have excitatory and inhibitory input from the same type of cells in the lateral geniculate nucleus (LGN), i.e., only from ON-center or OFF-center cells. The small size of the area where strong flank suppression occurred shows that inhibition comes from a few LGN cells rather than from a large pool of cells.A model for simple cell receptive fields presuming overlapping but acentric excitatory and inhibitory fields with input to both fields from either ON- or OFF-center LGN cells was tested by computer simulation and shown to fit the experimental data.The project was financially supported by the Norwegian Research Council for Science and the Humanities     

Receptive field organization of complex cells in cat striate cortex

Summary The receptive field organization of complex cells was studied by analyzing interaction effects between two stationary flashing light stimuli. One was placed in the most responsive part of the receptive field to produce activity against which effects of the other in different visual field positions could be determined.The receptive field was spatially organized into antagonistic center and flanks just like the fields of simple cells. However, both center and flanks were found within the receptive field area where a single slit evoked discharge. Center and flanks were elongated along the optimal stimulus orientation. The flanks were displaced from the center normal to optimal stimulus orientation.In the center, ON- and OFF-responses were usually about equal in strength and the maximum ON- and OFF-responses occurred in about the same position. This shows that complex cells are activated by input from both ON- and OFF-center cells in the lateral geniculate nucleus (LGN) where the receptive field centers of the LGN cells overlap closely. This explains most of the specific features of complex cells, e.g., the spatially overlapping ON- and OFF-zones, the large response field, the repetitive firing when a slit moves over the receptive field, and the marked non-linear spatial summation.Strong flank suppression occurred with both ON and OFF. The effects were usually stronger on one side of the center. Maximal suppression occurred on the same side with both ON and OFF. This is consistent with the interpretation that complex cells are inhibited by input from both LGN ON- and OFF-center cells with overlapping receptive field centers.A model presuming that complex cells have overlapping but acentric excitatory and inhibitory fields was tested by computer simulation and shown to fit the experimental data. This is the same model as presented for simple cells in the preceding paper (Heggelund 1980), except that the excitatory and inhibitory fields of simple cells have input from either ON- or OFF-center LGN cells, whereas in complex cells they have input from both types.The project was financially supported by the Norwegian Research Council for Science and Humanities     

Ontogenesis of receptive fields in the rabbit striate cortex

Summary The responses of rabbit striate cortex neurons to light or optic nerve shock were tested in 633 units in 54 rabbit pups 3–25 days of age. Units were driven by optic nerve shock at the youngest ages tested, but could not be driven by light until postnatal day eight. It was found that the symmetric receptive field types (concentric, uniform, motion) were present at or near the time of eye opening (10–11 days), while the asymmetric types (directional, simple, complex, oriented-directional) did not appear until several days later. All adult receptive field types were first seen at day 18. Until about day 20, cells with indefinite response properties were much more numerous than in the adult, and it is suggested thab cells with asymmetric receptive fields may differentiate out of the indefinite group. Development of visual response in the striate cortex is markedly retarded when compared to that in the superior colliculus.     

Analysis of retinal correspondence by studying receptive fields of rinocular single units in cat striate cortex

Summary The concept of corresponding retinal points was examined in terms of the binocular receptive fields of neurons in Area 17 of the cerebral cortex of the cat. Only a proportion of the binocular receptive field pairs can be accurately superimposed at the one time in a given plane. The fields which are not corresponding are said to show receptive field disparity. The attempt has been made to establish, on a quantitative basis, the parameters of the receptive field disparities that occur within 5° of the visual axis. A new method was used for defining the zero (vertical) meridian. Very effective paralysis of the extraocular muscles was achieved and the very small residual eye movements that occurred were regularly monitored so that corrections could be applied to the plotted positions of the receptive field pairs. The distribution of the receptive field disparities about the position of maximal correspondence has a range of about ±1.2° (S.D. 0.6°) in both the horizontal and vertical directions for fields in the vicinity of the visual axis. Panum's fusional area may represent the extent to which receptive fields in the one eye, all with the same visual direction, are linked to fellow members of a pair in the other eye over a range of receptive field disparities. A naso-temporal overlap of receptive fields occurs which is probably little if any more than can be accounted for on the basis of the disparity of receptive fields lying along the zero (vertical) meridian. When the extraocular muscles are paralyzed the eyes diverge and the binocular receptive field pairs are separated on the tangent screen. The distribution of the horizontal and vertical separations of the receptive field pairs have been examined.Selby Fellow of the Australian Academy of Sciences.     

Responses to moving slits by single units in cat striate cortex

Summary A quantitative study has been made of the responses to moving slit stimuli by single units in the cat striate cortex whose receptive fields lay within 5° of the visual axis. Special attention was given to finding the optimal stimulus parameters including slit width, length, orientation and speed. The analysis was largely based on averaged response vs. time histograms. Using the classification of simple and complex responses types, the units were further subdivided on the basis of the number of modes in the response and on the presence or absence of directional selectivity. Simple unimodal units with directional selectivity (SUDS) had the most specific stimulus requirements and nearly always had zero background activity. Complex units usually had a high level of background activity. SUDS units also showed a preference for horizontally- and vertically ****-orientated stimuli. Whenever the response survived reversal of contrast the directional selectivity remained independent of the change. Optimal stimulus speeds varied widely from unit to unit with a mean at 4°/sec: simple bimodal units and complex units tended to have higher optimal stimulus speeds and responded over a wider range of speeds than did simple unimodal units. While SUDS units with very small receptive fields tended to prefer slowly moving stimuli, in general there was no correlation between receptive field size and optimal stimulus speed.Selby Fellow of the Australian Academy of Sciences.     

Spatial summation by simple cells in the striate cortex of the cat

Summary Spatial summation has been studied in simple cells of the cat's visual cortex by examining the responses to pairs of lines. One line was placed in an ON region of the receptive field; the other was placed in an OFF region. When the luminances of the lines were modulated in anti-phase, the excitatory responses to the individual lines were almost synchronous. A simple cell's overt response to the composite stimulus was usually greater than the sum of the overt responses to the two components. The result could be explained by supposing that the underlying response was the linear sum of the excitatory signals but that an overt response occurred only when the underlying response exceeded a fixed threshold value. This was true even of simple cells which exhibited non-linearities of spatial summation, as judged from the waveforms of their responses to moving sinusoidal gratings. When the two lines were modulated in phase, the excitatory responses occurred in different halves of the temporal cycle. Some cells summed antagonistic signals linearly. The waveforms of their responses to moving sinusoidal gratings also implied linear spatial summation. However, other cells whose responses to moving gratings implied linearity of summation did not, in fact, sum antagonistic signals linearly. The excitatory responses evoked in a receptive field region were weaker than the inhibitory responses that could be evoked in the same region. The remaining cells did not sum antagonistic signals linearly. There was imperfect cancellation, resulting in the generation of ON-OFF response components. The excitatory responses evoked in a receptive field region were stronger than the inhibitory responses that could be evoked in the same region. These cells gave responses to sinusoidal gratings that did imply non-linear spatial summation.     

Magnification factor and receptive field size in foveal striate cortex of the monkey

Summary Receptive field size and magnification have been studied in striate cortex of awake, behaving rhesus monkeys at visual eccentricities in the range of 5–160 min. The major findings that emerge are (1) magnification in the foveola achieves values in the range of 30 mm/deg, (2) mean field size is not proportional to inverse magnification in contrast with previous reports, and (3) the product, magnification X aggregate field size, is greater in central vision than in peripheral vision. Thus, a point of light projected onto foveal retina is seen by larger numbers of striate cortical cells than a point of light projected onto peripheral retina.Implications of these findings for visual localization and two-point discrimination are discussed.Dedicated to Hermann RahnSupported by NIH grants EY02349 and 5 T32 EY07019     

Areal influences on complex cells in cat striate cortex: stimulus-specificity of width and length summation

Summary In single neurones recorded from the striate cortex of cats anaesthetized with N₂O/O₂/halothane, receptive field dimensions, length specificity and areal extent of drive were assessed for different classes of visual stimuli. Receptive fields were mapped as rectangular minimum response fields (MRFs). Spatial summation along the axis of preferred orientation was assessed: for moving bars whose length was varied (length summation); and for height variation of a square-wave grating patch against a uniform grey background, or a patch of moving texture against a stationary background of similar texture. In complementary tests a moving square-wave grating background was progressively occluded by a uniform grey foreground mask of variable height; or a mask of stationary texture of variable height progressively occluded a background of moving texture. In parallel measurements, the width of grating or textured patches or masks was varied whilst maintaining height constant. Broadly speaking, the areal influence of each class of stimulus was comparable, and distinct from extra-receptive field phenomena in evoking responses from within the receptive field, but not from surrounding areas. The masking paradigm provided the most sensitive measure of receptive field height and width. However, in some neurones length summation, the degree of endstopping, and the directional bias depended critically on the stimulus configuration used. Length summation tended to be more dramatic for short bars than for gratings. Length summation for texture was significantly more pronounced than for an oriented bar in special and in intermediate complex neurones. By contrast, endstopping was typically less intense for gratings than for bars, and least pronounced for texture. Because of stimulus specificity, complex neurones assigned to particular functional subgroups on the basis of their response to oriented bars may exhibit quite different patterns of behaviour for other classes of stimuli.     

Differential responsiveness of simple and complex cells in cat striate cortex to visual texture

Summary The responsiveness of 254 simple and complex striate cortical cells to various forms of static and dynamic textured visual stimuli was studied in cats, lightly anaesthetised with N₂O/O₂ mixtures supplemented with pentobarbitone.Simple cells were unresponsive to all forms of visual noise presented alone, although about 70% showed a change in responsiveness to conventional bar stimuli when these were presented on moving, rather than stationary, static-noise backgrounds. Bar responses were depressed by background texture motion in a majority of cells (54%), but were actually enhanced in a few instances (16%).In contrast, all complex cells were to some extent responsive to bars of static visual noise moving over stationary backgrounds of similar texture, or to motion of a whole field of static noise. The optimal velocity for noise was generally lower than for bar stimuli.Since moving noise backgrounds were excitatory for complex cells, they tended to reduce specific responses to bar stimulation; in addition, directional bias could be modified by direction and velocity of background motion.Complex cells fell into two overlapping groups as regards their relative sensitivity to light or dark bars and visual noise. Extreme examples were insensitive to conventional bar or edge stimuli while responding briskly to moving noise.In many complex cells, the preferred directions for motion of noise and of an optimally oriented black/white bar were dissimilar.The ocular dominance and the degree of binocular facilitation of some complex cells differed for bar stimuli and visual texture.Preliminary evidence suggests that the deep-layer complex cells (those tolerant of misalignment of line elements; Hammond and MacKay, 1976) were most sensitive to visual noise. Superficial-layer complex cells (those preferring alignment) were less responsive to noise.Only complex-type hypercomplex cells showed any response to visual noise.We conclude that, since simple cells are unresponsive to noise, they cannot provide the sole input to complex cells. The differences in the response of some complex cells to rectilinear and textured stimuli throw a new light on their rôle in cortical information-processing. In particular, it tells against the hypothesis that they act as a second stage in the abstraction of edge-orientation.     

Direction selectivity of simple cells in cat striate cortex to moving light bars

The response properties of 84 simple striate cells in anaesthetized (N2O/O2 supplemented with sodium pentobarbital) and paralyzed cats were examined quantitatively using narrow optimally-oriented light and dark bars moving at optimal velocities. Different cells gave two to five spatially-offset response peaks, the light bar and the dark bar response peaks alternating with one another. With only 5 exceptions, the cells had the same preferred direction for movement of the dark bar as for the light bar. Static-field plots were prepared from 32 of the 84 cells using stationary flashing bars. The receptive fields of different cells had from two to four subregions responding either at light on (ON subregion) or at light off (OFF subregion) although one cell had only a single subregion. In the preferred direction of stimulus movement cells gave either the same number of response peaks to moving bars as there were subregions or one additional response peak. The additional response peak, termed a boundary response, always occurred at the end of the sequence of response peaks and was always completely direction selective. The direction selectivities of the individual response peaks in the responses from 49 of the 84 cells were analyzed. To ensure that each response peak and the corresponding peak in the opposite direction both came from the same subregion, the 49 cells were selected on the basis of having a response in the nonpreferred direction sufficient for analysis and of having a stimulus velocity less than 2.5 degrees/s so as to avoid significant spatial shifts of the peaks due to response latencies. For all but two of the 49 cells, the response peaks in any given profile always showed a progressively greater degree of direction selectivity as the stimulus advanced from one subregion to the next, the first subregion giving the least directionally-selective response peak and the last subregion the most directionally-selective peak. This observation was independent of the direction of stimulus motion and of the particular sequence in which the ON and the OFF subregions were traversed by the stimulus. The response patterns observed experimentally have been correlated with theoretical response patterns based on the responses of lateral geniculate neurons.     

Spatial summation in the receptive field of simple cells in the cat striate cortex

Experimental Brain Research - Spatial summation was studied quantitatively through width response curves made with an optimally oriented test slit of variable width, and by comparing the response...     

Properties of end-zone inhibition of hypercomplex cells in cat striate cortex

Summary The response properties of 96 striate cells in anaesthetized and paralyzed cats were examined by using narrow optimally-oriented light bars moved in the preferred direction at optimal velocity. The bar was lengthened systematically at both ends to plot and analyze bilateral length-response curves. We found a linear relationship between the maximum slope of the inhibitory phase of the curve and the strength of the end-zone inhibition for both cell families: simple and B-cells. This observation indicates that the length of the two end-zones as given by a bilateral length-response curve is approximately constant regardless of the strength of the end-zone inhibition for a change in the strength of the inhibition from 10 to 100%.     

Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex

Summary We have characterized the speed of response of simple cells in cat striate cortex by the temporal phase of the response to bar and grating stimuli. Stimulation of the most responsive sub-region (either ON or OFF) in the receptive field with a 1 Hz temporally modulated bar elicited responses whose phase led the excitatory phase of the stimulus by about 25°. The response to stationary gratings whose contrast was sinusoidally modulated at 2 Hz also showed a phase lead. The differences in the phase of response of ON and OFF sub-regions exhibited a marked scatter about the expected value of 180°. The phase of response to both temporally modulated bars and laterally moving gratings advanced by 20–35° as the stimulus contrast was raised by a factor of 5.     

Nonlinear measurement and classification of receptive fields in cat retinal ganglion cells

Originally, modeling of ganglion-cell responses in cat was based mainly on linear analysis. This is satisfactory for those cells in which spatial summation of excitation is approximately linear (X-cells) but it fails for Y-cells, where summation has strong nonlinear components. Others have shown the utility of using sinusoidal analysis to study harmonic and intermodulation nonlinearities in the temporal frequency domain. We have used Wiener-kernel analysis to obtain directly both temporal and spatial impulse responses and their nonlinear interactions. From these, we were able to predict accurately the responses that a counterphase modulated grating elicited in both X-cells and Y-cells. In addition, we show that the first-order responses can measure the two-dimensional spatial features of the receptive field with high resolution. Thus, nonlinear analysis of responses to white-noise stimuli may be sufficient to both classify and measure the receptive fields of many different types of ganglion cells.     

Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex.

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)