Although the primary visual cortex (V1) is one of the most extensively studied areas of the primate brain, very little is known about how the far periphery of visual space is represented in this area. We characterized the physiological response properties of V1 neurons in anaesthetized marmoset monkeys, using high-contrast drifting gratings. Comparisons were made between cells with receptive fields located in three regions of V1, defined by eccentricity: central (3–5°), near peripheral (5–15°), and far peripheral (>50°). We found that orientation selectivity of individual cells was similar from the center to the far periphery. Nonetheless, the proportion of orientation-selective neurons was higher in central visual field representation than in the peripheral representations. In addition, there were similar proportions of cells representing all orientations, with the exception of the representation of the far periphery, where we detected a bias favoring near-horizontal orientations. The proportions of direction-selective cells were similar throughout V1. When the center/surround organization of the receptive fields was tested with gratings with varying diameters, we found that the population of neurons that was suppressed by large gratings was smaller in the far periphery, although the strength of suppression in these cells tended to be stronger. In addition, the ratio between the diameters of the excitatory centers and suppressive surrounds was similar across the entire visual field. These results suggest that, superimposed on the broad uniformity of V1, there are subtle physiological differences, which indicate that spatial information is processed differently in the central versus far peripheral visual fields.

The receptive fields of on- and off-center parasol cell mosaics independently tile the retina to ensure efficient sampling of visual space. A recent theoretical model represented the on- and off-center mosaics by noisy hexagonal lattices of slightly different density. When the two lattices are overlaid, long-range Moiré interference patterns are generated. These Moiré interference patterns have been suggested to drive the formation of highly structured orientation maps in visual cortex. Here, we show that noisy hexagonal lattices do not capture the spatial statistics of parasol cell mosaics. An alternative model based upon local exclusion zones, termed as the pairwise interaction point process (PIPP) model, generates patterns that are statistically indistinguishable from parasol cell mosaics. A key difference between the PIPP model and the hexagonal lattice model is that the PIPP model does not generate Moiré interference patterns, and hence stimulated orientation maps do not show any hexagonal structure. Finally, we estimate the spatial extent of spatial correlations in parasol cell mosaics to be only 200–350 μm, far less than that required to generate Moiré interference. We conclude that parasol cell mosaics are too disordered to drive the formation of highly structured orientation maps in visual cortex.

Monocular deprivation (MD) by lid suture is one of the classic paradigms for the study of developmental plasticity in the cerebral cortex, and we have detailed knowledge of its anatomical and physiological consequences as well as underlying molecular and cellular mechanisms. However, the effects of other forms of manipulating visual input through one eye on the functional architecture of the primary visual cortex (V1) have not yet been examined directly. We compared MD by lid suture with the effects of daily monocular lens wear using either a frosted lens or a neutral density (ND) filter. We used optical imaging of intrinsic signals and visually evoked potentials (VEPs) to assess responses in V1 to monocular stimulation. We found that loss of stimulus contrast through monocular frosted lens wear resulted in marked takeover of cortical territory by the nondeprived eye (NDE) similar to that caused by classic MD, and in virtual absence of orientation-selective responses following stimulation of the deprived eye (DE). Furthermore, amplitudes of VEPs in response to gratings of a range of spatial frequencies were significantly reduced in the DE compared to the NDE. In contrast, differences in luminance between two eyes caused by an ND filter in front of one eye did not affect ocular dominance and orientation maps, and there was no significant difference in the amplitude of VEPs elicited through the two eyes. Our results are consistent with previous electrophysiological studies in demonstrating that binocular pattern information is necessary to maintain normal functional maps in both eyes, while reduced luminance in one eye has little effect on the overall functional architecture and visual responses in V1.

Recordings were made from single neurons in area 18 of anesthetized cats (N2O/O2 mixture supplemented by continuous intravenous infusion of barbiturate) in which one optic nerve had been pressure blocked to selectively block conduction in the largest (Y-type) fibers. Cortical neurons were stimulated visually via the normal eye or via the eye with the pressure-blocked optic nerve (“Y-blocked eye”). Several properties of the receptive fields such as their spatial organization (S or C cells), orientation tuning, and the presence and strength of end-zone inhibition appear to be unaffected by removal of the Y input. By contrast, the removal of the Y input resulted in a small but significant reduction in the size of the discharge field and in the direction-selectivity index. In three respects, peak response discharge rate, eye dominance, and velocity sensitivity, removal of the Y input had strong and highly significant effects. Thus, the mean peak discharge frequency of responses evoked by the stimulation of binocular neurons via the Y-blocked eye was significantly lower than that of responses evoked by the stimulation via the normal eye. Accordingly, the eye-dominance histogram was shifted markedly towards the normal eye (more so than in the homologous experiment conducted on area 17 — Burke et al., 1992). Finally, the mean preferred velocity of responses of cells activated via the normal eye was in the vicinity of 145 deg/s, whereas for cells activated via the Y-blocked eye the value was about 35 deg/s. Overall, the results of the present study imply that (1) apart from Y-type excitatory input there are significant excitatory non-Y-inputs to area 18; these inputs at least partially consist of indirect X-type input relayed via area 17; (2) in neurons of area 18 that receive both Y-type and non-Y-type excitatory inputs, the Y-type input has a major influence on strength of the response and velocity sensitivity and a lesser influence on the direction selectivity and size of the discharge fields; and (3) area 18 contains mechanisms determining such receptive-field properties as S- or C-type organization, orientation tuning, and direction selectivity which can be accessed either by the Y input or by non-Y input.

Previous work has shown that small, stimulus-dependent changes in light absorption can be used to monitor cortical activity, and to provide detailed maps of ocular dominance and optimal stimulus orientation in the striate cortex of adult macaque monkeys (Blasdel & Salama, 1986; Ts'o et al., 1990). We now extend this approach to infant animals, in which we find many of the organizational features described previously in adults, including patch-like linear zones, singularities, and fractures (Blasdel, 1992b), in animals as young as 3/12 weeks of age. Indeed, the similarities between infant and adult patterns are more compelling than expected. Patterns of ocular dominance and orientation, for example, show many of the correlations described previously in adults, including a tendency for orientation specificity to decrease in the centers of ocular dominance columns, and for iso-orientation contours to cross the borders of ocular dominance columns at angles of 90 deg. In spite of these similarities, there are differences, one of which entails the strength of ocular dominance signals, which appear weaker in the younger animals and which increase steadily with age. Another, more striking, difference concerns the widths of ocular dominance columns, which increase by 20% during the first 3 months of life. Since the cortical surface area increases by a comparable amount, during the same time, this 20% expansion implies that growth occurs anisotropically, perpendicular to the ocular dominance columns, as the cortical surface expands. Since the observed patterns of orientation preference expand more slowly, at approximately half this rate, these results also imply that ocular dominance and orientation patterns change their relationship, and may even drift past one another, as young animals mature.

Mechanisms supporting orientation selectivity of cat striate cortical cells were studied by stimulation with two superimposed sine-wave gratings of different orientations. One grating (base) generated a discharge of known amplitude which could be modified by the second grating (mask). Masks presented at nonoptimal orientations usually reduced the base-generated response, but the degree of reduction varied widely between cells. Cells with narrow orientation tuning tended to be more susceptible to mask presence than broadly tuned cells; similarly, simple cells generally showed more response reduction than did complex cells.

The base and mask stimuli were drifted at different temporal frequencies which, in simple cells, permitted the identification of individual response components from each stimulus. This revealed that the reduction of the base response by the mask usually did not vary regularly with mask orientation, although response facilitation from the mask was orientation selective. In some sharply tuned simple cells, response reduction had clear local maxima near the limits of the cell's orientation-tuning function.

Response reduction resulted from a nearly pure rightward shift of the response versus log contrast function. The lowest mask contrast yielding reduction was within 0.1–0.3 log unit of the lowest contrast effective for excitation.

The temporal-frequency bandpass of the response-reduction mechanism resembled that of most cortical cells. The spatial-frequency bandpass was much broader than is typical for single cortical cells, spanning essentially the entire visual range of the cat.

These findings are compatible with a model in which weak intrinsic orientation-selective excitation is enhanced in two stages: (1) control of threshold by nonorientation-selective inhibition that is continuously dependent on stimulus contrast; and (2) in the more narrowly tuned cells, orientation-selective inhibition that has local maxima serving to increase the slope of the orientation-tuning function.

In an aseptic operation under surgical anesthesia, one optic nerve of a cat was exposed and subjected to pressure by means of a special cuff. The conduction of impulses through the pressurized region was monitored by means of electrodes which remained in the animal after the operation. The pressure was adjusted to selectively eliminate conduction in the largest fibers (Y-type) but not in the medium-size fibers (X-type). The conduction block is probably due to a demyelination and remains complete for about 3 weeks. Within 2 weeks after the pressure-block operation, recordings were made from single neurons in the striate cortex (area 17, area VI) of the cat anesthetized with N2O/O2 mixture supplemented by continuous intravenous infusion of barbiturate. Neurons were activated visually via the normal eye and via the eye with the pressure-blocked optic nerve (“Y-blocked eye”). Several properties of the receptive fields of single neurons in area 17 such as S (simple) or C (complex) type of receptive-field organization, size of discharge fields, orientation tuning, direction-selectivity indices, and end-zone inhibition appear to be unaffected by removal of the Y-type input. On the other hand, the peak discharge rates to stimuli presented via the Y-blocked eye were significantly lower than those to stimuli presented via the normal eye. As a result, the eye-dominance histogram was shifted markedly towards the normal eye implying that there is a significant excitatory Y-type input to area 17. In a substantial proportion of area 17 neurons, this input converges onto the cells which receive also non-Y-type inputs. In one respect, velocity sensitivity, removal of the Y input had a weak but significant effect. In particular, C (but not S) cells when activated via the normal eye responded optimally at slightly higher stimulus velocities than when activated via the Y-blocked eye. These results suggest that the Y input makes a distinct contribution to velocity sensitivity in area 17 but only in C-type neurons. Overall, our results lead us to the conclusion that the Y-type input to the striate cortex of the cat makes a significant contribution to the strength of the excitatory response of many neurons in this area. However, the contributions of Y-type input to the mechanism(s) underlying many of the receptive-field properties of neurons in this area are not distinguishable from those of the non-Y-type visual inputs.

We have employed the tetrode technique, which allows accurate discrimination of individual neuronal spike trains from multiunit recordings, in order to examine the variation of orientation selectivity among local groups of neurons. We recorded a total of 321 cells from 62 sites in area 17 of halothane-anesthetized cats; each site contained between three to ten neurons that were estimated to be less than 65 μm away from the tetrode tip. For each cell, we determined the orientation tuning in response to moving bars. Of the cells tested, 8.4% were unresponsive, 22.7% had no preferential response to any particular orientation, while 68.8% were tuned. The average difference in preferred orientation between cell pairs recorded at the same site was 10.7 deg, but the variance in preferred orientation differences differed significantly among sites. Some clusters of cells exhibited the same or nearly the same orientation preference, while others had orientation preferences that differed by as much as 90 deg. Our data demonstrate that the tuning for orientation is more heterogeneously distributed at a local level than previous studies have suggested.

The purpose of this investigation was to analyze the influence of stimulus orientation on the responses of individual neurons in the monkey's lateral geniculate nucleus (LGN). Our specific goals were to assess the prevalence and the degree of orientation tuning in the monkey LGN and to determine if the preferred stimulus orientations of LGN neurons varied as a function of receptive-field position. The primary motivation for this research was to gain insight into the receptive-field configuration of LGN neurons and consequently into the neural mechanisms which determine the spatial organization of LGN receptive fields in primates.

In both the parvocellular and magnocellular layers, the responses of the majority of individual neurons to sine-wave gratings varied as a function of stimulus orientation. The influence of stimulus orientation was, however, highly dependent on the spatial characteristics of the stimulus; the greatest degree of orientation bias was observed for spatial frequencies higher than the cell's optimal spatial frequency. On a population basis, the degree of orientation bias was similar for all major classes of LGN neurons (e.g. ON vs. OFF center; parvocellular vs. magnocellular) and did not vary systematically with receptive-field eccentricity. At a given receptive-field location, LGN neurons, particularly cells in the parvocellular laminae, tended to prefer either radially oriented stimuli or stimuli oriented more horizontally than their polar axis. Our analyses of the orientation-dependent changes in spatial-frequency response functions, which was based on the Soodak et al., (1987; Soodak, 1986) two-dimensional, difference-of-Gaussian receptive-field model, suggested that the orientation bias in LGN neurons was due to an elongation of the receptive-field center mechanism which in some cases appeared to consist of multiple subunits. Direct comparisons of the orientation-tuning characteristics of LGN cells and their retinal inputs (S potentials) indicated that the orientation bias in the monkey LGN reflects primarily the functional properties of individual retinal ganglion cells. We conclude that orientation sensitivity is a significant property of subcortical neurons in the primate's geniculo-cortical pathway.

We evaluated the dynamic aspects of the orientation tuning of the input to cat visual cortical neurons by analyzing the postsynaptic potentials (PSPs) evoked by flashing bars of light. The PSPs were recorded using in vivo whole-cell technique, and we analyzed the orientation tuning during subsequent temporal windows after stimulus onset and offset. Our results show that the amplitudes of the postsynaptic potential are reliably tuned to orientation and matching that of the spike responses only during certain temporal windows. During the first 100 ms after stimulus presentation, orientation tuning of the membrane potential underwent regular changes. Within particular intervals, orientation tuning of the input was much sharper than that estimated according to the whole response. In most cells, optimal orientation was usually stable over the whole period. In several cells which had a second hump of EPSPs in the response, this second hump was tuned to the same orientation as the first one, but always showed sharper tuning. Estimation of the integration time revealed sufficient delay between the appearance of EPSPs and spikes, to let inhibition influence spike generation. These results show that orientation selectivity of the input to cortical cells is a dynamic function, and also indicate the possibility of temporal coding in the visual system.

One striking transformation in response properties that occurs in the geniculo-cortical pathway is the appearance of a high degree of orientation selectivity in the cortex. This property may be conceived as arising purely from the excitatory inputs to the cell, as being structured largely by the inhibition a cortical cell receives or could be due to a combination of the two. We have studied the contributions of excitatory and inhibitory inputs to cortical cells' orientation selectivity by analyzing the postsynaptic potentials evoked in cat striate neurones by flashing stimuli of different orientations. We made these recordings using the in vivo whole-cell technique (Xing Pei et al., 1991), which provides more stable and reliable results than classical intracellular recording methods. Our results show that the cat striate cortex exhibits a variety of mechanisms to achieve orientation selectivity. Orientation selectivity of a particular cell can be created by excitatory, by inhibitory, or by a combination of both mechanisms.

There is controversy in the literature concerning whether or not neurons in the cat's posteromedial lateral suprasylvian (PMLS) visual cortex are orientation selective. Previous studies that have tested cells with simple bar stimuli have found that few, if any, PMLS cells are orientation selective. Conversely, studies that have used repetitive stimuli such as gratings have found that most or all PMLS cells are orientation selective. It is not known whether this difference in results is due to the stimuli used or the laboratories using them. The present experiments were designed to answer this question by testing individual PMLS neurons for orientation sensitivity with both bar and grating stimuli. Using quantitative response measures, we found that most PMLS neurons respond well enough to stationary flashed stimuli to use such stimuli to test for orientation sensitivity. On the basis of these tests, we found that about 85% of the cells with well-defined receptive fields are orientation sensitive to flashed gratings, and a similar percentage are orientation sensitive to flashed bars. About 80% of the cells were orientation sensitive to both types of stimuli. The preferred orientations typically were similar for the two tests, and they were orthogonal to the preferred direction of movement. The strength of the orientation sensitivity (measured as the ratio of discharge to the preferred and nonpreferred orientations) was similar to both types of stimuli. However, the width of the orientation tuning curves was systematically broader to bars than to gratings. Several hypotheses are considered as to why previous studies using bars failed to find evidence for orientation sensitivity. In addition, a mechanism for the difference in orientation tuning to bars and gratings is suggested.

Bistratified (BS) ganglion cells have long been recognized in vertebrate retina. Thirty years ago, it became clear that bistratification allows the integration of ON and OFF retinal pathways to produce contrast-independent responses in ganglion cells. Best studied is the type 1 bistratified (BS1) ganglion cell of rabbit retina, the physiologically well-characterized ON-OFF directionally selective (DS) ganglion cell, which is co-stratified with the two types of starburst amacrine (SA) cells in sublaminae a and b of the inner plexiform layer (IPL). DS responses have recently been documented in the latter. In this report, BS1 cells are further studied and are used as “fiducials” to characterize a second type of BS ganglion cell. An example of a possible third type is shown to be distinct from examples of BS1 and BS2 cells. All three have two distinct, narrowly stratified arborizations, one in sublamina a and one in sublamina b. All have similar dimensions, except for their dendritic trees, differing also in branching pattern. BS1 cells have compact, regular, highly branched trees; BS2 cells have significantly larger, more sparsely branched, irregular, radiate trees; the proposed BS3 type is intermediate in field size, and its branching pattern is different from the first two. BS2 and BS3 cells are co-stratified, branching nearer to the margins of the IPL, out of range of SA cells. In a previous report by others, illustrating the morphology of intracellularly stained ganglion cells, one example each of both “orientation-selective” ganglion cells and “uniformity detectors” resembles the BS2 cell. A rationale is presented for correlating BS2 cells with uniformity detectors.

Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.

Within the visual cortex of several mammalian species, more circuitry is devoted to the representation of vertical and horizontal orientations than oblique orientations. The sensitivity of this representation of orientation preference to visual experience during cortical maturation and the overabundance of cardinal contours in the environment suggest that vision promotes the development of this cortical anisotropy. We tested this idea by measuring the distribution of cortical orientation preference and the degree of orientation selectivity in developing normal and dark-reared ferrets using intrinsic signal optical imaging. The area of the angle map of orientation preference representing cardinal and oblique orientations was determined; in addition, orientation selectivity indices were computed separately for cardinal and oblique difference images. In normal juvenile animals, we confirm a small, but statistically significant overrepresentation of near horizontal orientations in the cortical angle map. However, the degree of anisotropy did not increase in the weeks that followed eye opening when orientation selectivity matured; rather, it decreased. In dark-reared ferrets, an even greater cortical anisotropy emerged, but angle maps in these animals developed an apparently anomalous overrepresentation of near vertical orientations. Thus, the overrepresentation of cardinal orientations in the visual cortex does not require experience with an anisotropic visual environment; indeed, cortical anisotropy can develop in the complete absence of vision. These observations suggest that the role of visual experience in cortical maturation is to promote the isotropic representation of orientation preference.

Orientation selectivity is one of the most conspicuous receptive-field (RF) properties that distinguishes neurons in the striate cortex from those in the lateral geniculate nucleus (LGN). It has been suggested that orientation selectivity arises from an elongated array of feedforward LGN inputs (Hubel & Wiesel, 1962). Others have argued that cortical mechanisms underlie orientation selectivity (e.g. Sillito, 1975; Somers et al., 1995). However, isolation of each mechanism is experimentally difficult and no single study has analyzed both processes simultaneously to address their relative roles. An alternative approach, which we have employed in this study, is to examine the relative contributions of linear and nonlinear mechanisms in sharpening orientation tuning. Since the input stage of simple cells is remarkably linear, the nonlinear contribution can be attributed solely to cortical factors. Therefore, if the nonlinear component is substantial compared to the linear contribution, it can be concluded that cortical factors play a prominent role in sharpening orientation tuning. To obtain the linear contribution, we first measure RF profiles of simple cells in the cat's striate cortex using a binary m-sequence noise stimulus. Then, based on linear spatial summation of the RF profile, we obtain a predicted orientation-tuning curve, which represents the linear contribution. The nonlinear contribution is estimated as the difference between the predicted tuning curve and that measured with drifting sinusoidal gratings. We find that measured tuning curves are generally more sharply tuned for orientation than predicted curves, which indicates that the linear mechanism is not enough to account for the sharpness of orientation-tuning. Therefore, cortical factors must play an important role in sharpening orientation tuning of simple cells. We also examine the relationship of RF shape (subregion aspect ratio) and size (subregion length and width) to orientation-tuning halfwidth. As expected, predicted tuning halfwidths are found to depend strongly on both subregion length and subregion aspect ratio. However, we find that measured tuning halfwidths show only a weak correlation with subregion aspect ratio, and no significant correlation with RF length and width. These results suggest that cortical mechanisms not only serve to sharpen orientation tuning, but also serve to make orientation tuning less dependent on the size and shape of the RF. This ensures that orientation is represented equally well regardless of RF size and shape.

We report results of numerical simulations for a model of generation of orientation selectivity in macaque striate cortex. In contrast to previous models, where the initial orientation bias is generated by convergent geniculate input to simple cells and subsequently sharpened by lateral circuits, our approach is based on anisotropic intracortical excitatory connections which provide both the initial orientation bias and its subsequent amplification. Our study shows that the emerging response properties are similar to the response properties that are observed experimentally, hence the hypothesis of an intracortical generation of orientation bias is a sensible alternative to the notion of an afferent bias by convergent geniculocortical projection patterns. In contrast to models based on an afferent orientation bias, however, the “intracortical hypothesis” predicts that orientation tuning gradually evolves from an initially nonoriented response and a complete loss of orientation tuning when the recurrent excitation is blocked, but new experiments must be designed to unambiguously decide between both hypotheses.

Direction selectivity and orientation selectivity were examined in the direction-selective (DS) and orientation- selective (OS) ganglion cells in the rabbit retina. Spike activities were recorded in vivo using tungsten-in-glass electrodes. Three types of visual stimuli (flashing slit, moving edges behind a slit, and whole-field drifting gratings) were used to distinguish these attributes. Fourier analysis was performed on data obtained using drifting gratings as proposed by Worgotter and Eysel (1987). Results from both angular and Fourier (polar angle frequency) domains were consistent. DS cells had strong directional components and varying strength of orientational components; they also had intact inhibitory surrounds. The phase of the biased orientation did not have a consistent relationship with the preferred direction. OS cells had predominant orientational components and very weak directional components. We conclude that the orientation bias does not contribute to the generation of direction selectivity, and that the mechanism of this bias of DS cells is rather different from the mechanism that generates orientation selectivity in rabbit OS cells. There are indications that it is similar to the mechanism shown to cause orientation bias in cat concentric cells.