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.     

Spatiotemporal organization of cat lateral geniculate receptive fields.

Spatial and temporal properties of LGN receptive fields were studied by flashing a small bar of light across the field in 28 discrete steps. The flashes at each of the spatial positions were used to produce 28 PST histograms. These histograms were in turn displayed as a plane, with space on the chi axis, time on the psi axis, and probability of firing on the zota axis. These response planes demonstrate that the terms on, off, center, and surround do not adequately describe when the simplest LGN receptive field. We, therefore, introduce a new terminology describing the four major spatiotemporal components of LGN fields. The primary excitatory (PE) domain corresponds to the strongest excitatory response, the secondary excitatory (SE) domain corresponds to the second-strongest excitatory domain, the primary inhibitory (PI) domain corresponds to the strongest inhibitory domain and, finally, the secondary inhibitory (SI) domain corresponds to the second-strongest inhibitory domain. Based on the arrangement of these four domains, it is possible to divide LGN fields into four major categories: 1) homogeneous-on, on-center receptive fields which have a spatially homogeneous distribution of domains; 2) homogeneous-off, off-center receptive fields which have a spatially homogeneous distribution of domains; 3) heterogeneous-on, on-center receptive fields which have a spatially heterogeneous distribution of domains; and 4) heterogeneous-off, off-center receptive fields which have a spatially heterogeneous distribution of domains; 3) heterogeneous-on, on-center receptive fields which have a spatially heterogeneous distribution of domains; and 4) heterogeneous-off, off-center receptive fields which have a spatially heterogeneous distribution of domains. Using grating, it can be demonstrated that our heterogeneous/homogeneous fields correspond to X/Y fields, respectively. These data lead us to suggest that retinal PE domains generage LGN PE and SI domains, while retinal SE domains generate LGN SE and SI domains.     

Spatial structure and symmetry of simple-cell receptive fields in macaque primary visual cortex

I present measurements of the spatial structure of simple-cell receptive fields in macaque primary visual cortex (area V1). Similar to previous findings in cat area 17, the spatial profile of simple-cell receptive fields in the macaque is well described by two-dimensional Gabor functions. A population analysis reveals that the distribution of spatial profiles in primary visual cortex lies approximately on a one-parameter family of filter shapes. Surprisingly, the receptive fields cluster into even- and odd-symmetry classes with a tendency for neurons that are well tuned in orientation and spatial frequency to have odd-symmetric receptive fields. The filter shapes predicted by two recent theories of simple-cell receptive field function, independent component analysis and sparse coding, are compared with the data. Both theories predict receptive fields with a larger number of subfields than observed in the experimental data. In addition, these theories do not generate receptive fields that are broadly tuned in orientation and low-pass in spatial frequency, which are commonly seen in monkey V1. The implications of these results for our understanding of image coding and representation in primary visual cortex are discussed.     

Position-specific adaptation in simple cell receptive fields of the cat striate cortex.

1. Responses of simple cells in cat striate cortex were studied with flashed light-slit stimuli. The responses to bars flashed in different positions in the receptive field were assessed quantitatively before and after periods of prolonged stimulation of one small region. This type of prolonged stimulation resulted in reduced responsivity over a limited zone within the simple cell receptive field. 2. The adaptation-induced responsivity decrement was generally confined to the receptive-field subregion that was adapted (either ON or OFF). Prolonged stimulation within an ON region did not usually result in adaptation effects that spread into neighboring OFF regions. Furthermore, the adaptation-induced response decrement did not necessarily spread throughout the subregion in which the adapting stimulus was presented. The adaptation effects from prolonged stimulation at a single receptive-field position spread throughout the subregion in nearly one-half of the 25 cells examined for position-specific adaptation. Another subpopulation of neurons (n = 12) displayed adaptation effects that spread through only one-half of the subregion, whereas in two neurons the spread of the adaptation effect was even more restricted and encompassed only one-fourth of the subregion. 3. The spread of adaptation was not systematically related to the size of the stimulus presented, the size of the receptive field, or the magnitude of the adaptation-induced response decrements but was significantly correlated with the spatial wavelength of the cell (the reciprocal of the cell's preferred spatial frequency) and with the size of the subregion in which the adapting stimulus was presented. Cells with large receptive-field subregions and long wave-lengths showed adaptation effects that spread further than those of cells with small subregions. 4. The adaptation effects from repeated stimulation at a single receptive-field position did not spread symmetrically across the receptive field, and the preferred direction of motion for a given cell indicated the direction of the asymmetric spread of the adaptation. Receptive-field positions that would be stimulated by a light slit originating at the point of adaptation and moving in the preferred direction (preferred side) showed greater adaptation-induced response decrements than did receptive-field positions that would be stimulated by a light slit moving in the opposite direction from the point of adaptation (nonpreferred side). There was significant enhancement of responses at some receptive-field positions on the nonpreferred side of the point of adaptation.(ABSTRACT TRUNCATED AT 400 WORDS)     

'Top-down' influences of ipsilateral or contralateral postero-temporal visual cortices on the extra-classical receptive fields of neurons in cat's striate cortex

In anesthetized and immobilized domestic cats, we have studied the effects of brief reversible inactivation (by cooling to 10 degrees C) of the ipsilateral or contralateral postero-temporal visual (PTV) cortices on: 1) the magnitude of spike-responses of neurons in striate cortex (cytoarchitectonic area 17, area V1) to optimized sine-wave modulated contrast-luminosity gratings confined to the classical receptive fields (CRFs) and 2) the relative strengths of modulation of CRF-induced spike-responses by gratings extending into the extra-classical receptive field (ECRF). Consistent with our previous reports (Bardy et al., 2006; Huang et al., 2007), inactivation of ipsilateral PTV cortex (presumed homologue of primate infero-temporal cortex) resulted in significant reversible changes (almost all substantial reductions) in the magnitude of spike-responses to CRF-confined stimuli in about half of the V1 neurones. Similarly, in half of the present sample, inactivation of ipsilateral PTV cortex resulted in significant reversible changes (in over 70% of cases, reduction) in the relative strength of ECRF modulation of the CRF-induced spike-responses. By contrast, despite the fact that receptive fields of all V1 cells tested were located within 5 degrees of representation of the zero vertical meridian, inactivation of contralateral PTV cortex only rarely resulted in significant (yet invariably small) changes in the magnitude of spike-responses to CRF-confined stimuli or significant (again invariably small) changes in the relative strength of ECRF modulation of spike-responses. Thus, the ipsilateral, but not contralateral, 'higher-order' visual cortical areas make significant contribution not only to the magnitude of CRF-induced spike-responses but also to the relative strengths of ECRF-induced modulation of the spike-responses of V1 neurons. Therefore, the feedback signals originating from the ipsilateral higher-order cortical areas appear to make an important contribution to contextual modulation of responses of neurons in the primary visual cortices.     

A model for self-organization of receptive fields and orientation-selective columns in the striate cortex.

In area 17 of the cat visual cortex, simple cells form a hypercolumn in which the optimum orientation from one column to the next gradually changes, composing a complete set of orientation-selective columns (orientation column). This article proposes a model for the development of the bar-shape receptive field of a simple cell and the self-organization of orientation columns. The receptive field of an immature cell in area 17 is assumed to be composed of a circular center and surrounding regions whose synaptic modification rules are different. The synaptic modifications also differ depending on whether the response of a cell is locally maximal or not. The modification of the efficacy of both excitatory and inhibitory synapses is determined according to the combination of activities of the visual cortical cell and the lateral geniculate neuron. The simulation of this model shows the development of the bar-shape receptive field and the self-organization of orientation columns of more than one cycle from 0 degrees to 180 degrees. The abnormal presentations of visual stimuli to this model result in the abnormal development of the orientation column. These simulation results are in good agreement with reported experimental results. Possible neural circuits to achieve this model are proposed. The neural circuits for the synaptic modification are built on the assumption that cortical cells release molecules to modify synaptic efficacies. The neural circuits for the detection of the maximally responding cell are composed of two kinds of inhibitory interneurons. The bar-shape receptive field is assumed to be a consequence of the topographic projection of visual afferents, radial branching of dendrites of a simple cell, and the existence of an inhibitory interneuron.     

Quantification of excitatory receptive fields of complex neurones in cat striate cortex

To use sensory information from the skin to guide motor behaviour the central nervous system must transform sensory coordinates into movement coordinates. As yet, the basic principles of this crucial neural computation are unclear. One motor system suitable as a model for the study of such transformations is the spinal withdrawal reflex system. The spatial organization of the cutaneous input to these reflexes has been characterized, and we now introduce a novel method of motion analysis permitting a quantitative analysis of the spatial input-output relationship in this motor system. For each muscle studied, a mirror-image relationship was found between the spatial distribution of reflex gain for cutaneous input and the pattern of cutaneous unloading ensuing on contraction. Thus, there is an imprint of the movement pattern on this motor system permitting effective sensorimotor transformation. This imprint may indicate the presence of a learning process which utilizes the sensory feedback ensuing on muscle contraction.     

The two-dimensional spectral structure of simple receptive fields in cat striate cortex

1. A quantitative, general purpose method was developed for measuring the responses of visual neurons to stimuli distributed with high resolution over the two-dimensional (2D) spatial frequency domain. The stimuli consisted of drifting sinusoidal gratings of nonsaturating contrasts whose spatial frequency and orientation were drawn in random order from a 16 X 16 array of coordinates covering each neuron's responsive area. This method was applied to a population of 36 simple cells in area 17 of cat. 2. The response of each simple cell to drifting sinusoidal gratings appeared as a rectified sinusoidal modulation of the spike frequency. The degree of rectification varied from cell to cell, but for each cell, the form of the response was constant irrespective of stimulus spatial frequency, orientation, or contrast. The amplitude of the average response at the stimulus temporal frequency was used as the response metric at all spectral coordinates. Variations in this amplitude over two spectral dimensions forms a surface that we call the 2D spectral response profile. 3. For each cell, the 2D spectral response profile was localized to a limited region of the complete 2D spatial frequency domain. In bidirectionally responsive cells, there were two lobes in the surface disposed with mirror symmetry about the origin. In all cells, each lobe exhibited a single maximum and the response decayed smoothly in every direction away from the maximum. Isoresponse amplitude contours were elliptical and often, but not always, elongated about an axis of symmetry passing through the origin. 4. We tested the hypothesis that orientation and spatial frequency tuning are independent by forming scaled radial and angular sections through 2D spectral response profiles. In virtually every case polar separability did not obtain, that is, orientation selectivity depended on spatial frequency and vice versa. 5. In contrast, more than half the cells had 2D spectral response profiles that were Cartesian separable. The 2D spectral response profiles of most of the remaining cells were neither polar nor Cartesian separable, because the response profiles were elongated about an axis of symmetry that did not pass through the origin. 6. These results are discussed in terms of the constraints they place on models of the contributions simple cells make toward the neural representation of images.     

The two-dimensional spatial structure of simple receptive fields in cat striate cortex

1. A reverse correlation (6, 8, 25, 35) method is developed that allows quantitative determination of visual receptive-field structure in two spatial dimensions. This method is applied to simple cells in the cat striate cortex. 2. It is demonstrated that the reverse correlation method yields results with several desirable properties, including convergence and reproducibility independent of modest changes in stimulus parameters. 3. In contrast to results obtained with moving stimuli, we find that the bright and dark excitatory subregions in simple receptive fields do not overlap to any great extent. This difference in results may be attributed to confounding the independent variables space and time when using moving stimuli. 4. All simple receptive fields have subregions that vary smoothly in all directions in space. There are no sharp transitions either between excitatory subregions or between subregions and the area surrounding the receptive field. 5. Simple receptive fields vary both in the number of subregions observed, in the elongation of each subregion, and in the overall elongation of the field. In contrast with results obtained using moving stimuli, we find that subregions within a given receptive field need not be the same length. 6. The hypothesis that simple receptive fields can be modeled as either even symmetric or odd symmetric about a central axis is evaluated. This hypothesis is found to be false in general. Most simple receptive fields are neither even symmetric nor odd symmetric. 7. The hypothesis that simple receptive fields can be modeled as the product of a width response profile and an orthogonal length response profile (Cartesian separability) is evaluated. This hypothesis is found to be true for only approximately 50% of the cells in our sample.     

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)     

Color vision mechanisms in monkey striate cortex: dual-opponent cells with concentric receptive fields.

1. I have recorded with tungsten microelectrodes from single cells in the monkey's visual cortex and have specifically studied those neurons which were sensitive to the color of the stimulus. In the primate striate cortex there are four classes of color-coded cells. The cells described in this paper have concentric receptive fields with one red-green opponent-color system in the field center and the opposite organization in the surround. These dual-opponent cells were nost sensitive to the simultaneous presentation of two different colors, one covering the field center and the other illuminating the surround. They are probable involved in the perception of simultaneous color-contrast phenomena. 2. Spectral sensitivity curves revealed that both the field centers and the surrounds received opposite types of inputs from red-sensitive and green-sensitive cones. None of the cells tested had inputs from rods. 3. Area-sensitivity curves showed that peripheral suppression was present for both phases of the center opponent-color system. The boundary between the center and the surround was the same for both sets of opponent systems. Some cells had "silent" surrounds, which did not respond to annular stimuli. 4. Multiple-unit recordings from a concentric cell and one of its presumed afferents yielded information regarding its possible synaptic inputs. In some cases the cells appeared to receive contacts from red/green opponent-color geniculated fibers with circular receptive fields that lacked an antagonistic surround (similar to Wiesel and Hubel's (37) type II class). In other instances the afferents had on-center, off surround receptive fields or the reverse, but received inputs from only one cone type, either red or green (similar to Wiesel and Hubel's type III class). 5. Concentric cells were always driven by only one eye. 6. The laminar distribution of these cells was limited almost entirely to layer IV and its subdivisions. 7. The cumulative evidence presented in this paper indicates that the concentric cells probably received direct geniculate inputs and, therefore, they are the first cortical stage in the integration of color-contrast information.     

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.