Simulation Studies of the Role of Intracortical Inhibition in the Formation of Sensitivity to Cross-Shaped Figures

The receptive fields of detector neurons for cross-shaped figures in the visual cortex were modeled in conditions of blockade of intracortical inhibition. The tuning of simulated neurons was compared with and without inhibition in the receptive field. In a simulated detector with convergence from two orientation detectors, acute tuning to the cross widened in the absence of inhibition, becoming invariant to the shape and orientation of the cross. A detector based on the disinhibition mechanism lost cross sensitivity when inhibition was blocked and became a detector for the orientation of a single bar. A model of a receptive field in which the inhibitory zones mask the tuning to a cross-shaped figure and in which blockade of inhibition affects only sensitivity is also proposed. We identified which of the properties of receptive field (configuration, location, zone weightings) allow them to simulate the properties of cat visual cortex field 17 neurons, these being sensitive to the shape and orientation of cross-shaped figures. __________ Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 54, No. 6, pp. 767–775 November–December, 2004.     

Model Studies of the Mechanisms of Tuning of Visual Cortex Neurons to Incomplete Cross-Shaped Figures

Numerical simulation modeling of the receptive fields of visual cortex neurons able to detect cross-shaped figures with masked central or peripheral areas was performed. Receptive field models of two types were considered: those with antagonistic and cooperative interactions between the center and the periphery. Model neurons with receptive fields with reciprocal (antagonistic) interactions produced greater responses to peripheral or central crosses than to complete crosses. Studies using the model showed that the basis of this type of tuning could be provided by a disinhibition mechanism: blockade of the inhibitory zones in the center or periphery of the receptive field by activation of a lateral disinhibitory zone. A model with cooperative interactions between the center and periphery of the receptive field was also studied, in which responses to complete crosses were summed from the responses to the peripheral and central parts. Tuning of these model receptive fields was comparable to the sensitivity of real visual cortex neurons to the shape, size, and orientation of figures. The properties of model receptive fields (configuration, localization, and weightings of the various zones) allowing simulation of the properties of cat visual cortex field 17 neurons sensitive to the orientation and configuration of incomplete cross-shaped figures were identified.     

Stimulation of non-classical receptive field enhances orientation selectivity in the cat

We have investigated how the nonclassical receptive field (nCRF) affects dynamic orientation selectivity of cells in the primary visual cortex (V1) in anaesthetized and paralysed cats using the reverse correlation method. We found that tuning to the orientation of the test stimulus depends on the size of the stimulation area. A significant sharpening of orientation tuning was induced by nCRF stimulation, with the magnitude of the effect increasing with the size of stimulation. The effect of the nCRF on the temporal dynamics of orientation tuning was also investigated by examining the tuning over a range of delays from stimulus onset. We found small but detectable changes in both the preferred orientation and the bandwidth of tuning over time when the classical receptive field (CRF) was stimulated alone. Stimulation in nCRF significantly increased the magnitude of these temporal changes. Thus, nCRF stimulation not only enhances the overall orientation selectivity, but also enriches the temporal dynamics of cortical neurones, which may increase the computational power of the visual cortex in information processing.     

Receptive Fields of Bar and Cross-Shaped Figure Detectors in Classical and Combined Mapping

Connections between the excitatory and inhibitory zones of the receptive fields of neurons sensitive to the orientations of single bars and cross-shaped figures in the primary visual cortex were studied by classical and combined mapping. Factor and correlation analysis revealed different relationships between the main characteristics of neurons and their receptive fields for bar and cross detectors. Factor analysis of these connections showed that variables with the greatest weightings, combined into a single factor, were different for different detectors. In bar detectors, there was a direct correlational relationship between background activity and the weighting characteristics of the excitatory and inhibitory zones of their receptive fields. In cross-shaped figure detectors, the indexes of inhibition were positively related to the index of sensitivity to the figure, the characteristics of the excitatory zones of the receptive field, and background activity. In these detectors, increases in the area and weighting of additional receptive field excitatory zones in combined mapping were significantly greater than in bar detectors. The question of the difference in the mechanisms forming the receptive fields of bar and cross-shaped figure detectors, for which direct and recurrent horizontal inhibitory connections with surrounding neurons are more important, is discussed.     

Dynamic changes in the tuning of striate neurons to the shapes of cross-shaped figures

Time slice analysis was used to study the dynamics of tuning to the shapes of cross-shaped figures flashing in the receptive fields of 83 neurons in the primary visual cortex (field 17) of the cat brain. Tuning was assessed in terms of the numbers of spikes in the overall response and its sequential 20-msec fragments. Only 11.7% of neurons produced reproducibly developing spike responses to a given shape (defined as the angle between the lines), i.e., had a preferred cross-shaped figure. In the remaining cases (88.3%), tuning of neurons to the shape of the cross showed dynamic changes. In 7.2% of cases, changes in the preferred shape of the cross occurred monophasically; changes were biphasic in 27.0% of cases, while in the remaining 54.1% of cases, the dynamics in changes in the preferred cross shape were undulatory. The tuning of receptive field zones is assessed as the cause of these effects and their difference from the previously observed dynamics of preferred orientations of single bars and cross-shaped figures; the functional significance of these effects is also discussed.Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 89, No. 10, pp. 1216–1225, October, 2003.     

The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat.

1. The iontophoretic application of the GABA antagonist bicuculline to simple and complex cells in the striate cortex of the cat produced extensive modifications of receptive field properties. These modifications appear to relate to a block or reduction of GABA-mediated intracortical inhibitory influences acting on the cells examined. 2. For simple cells the effects of bicuculline on receptive field properties involved a loss of the subdivision of the receptive field into antagonistic "on" and "off" regions, a reduction in orientation specificity and a reduction or elimination of directional specificity. 3. The effect on the "on" and "off" subdivisions of the simple cell receptive field was such that all stationary flashing stimuli, whether covering the whole receptive field, or located within the receptive field over a previously determined "on" or "off" region, resulted in an "on and off" response. 4. The orientation specificity of complex cells was reduced during the application of bicuculline such that in many cases the original specificity of the cell was virtually lost with the response to the orientation at 90 degrees to the optimal being of similar magnitude to the optimal. The directional specificity of complex cells was generally less affected than that of simple cells. Often when large changes in orientation specificity were observed the directional specificity was relatively unaffected. 5. For some cells apparently showing to all visual stimuli only inhibitory responses, the application of bicuculline resulted in the appearance of excitatory responses. 6. In all cases receptive field properties reverted to the original state after termination of the bicuculline application. It was not generally possible to duplicate the effects of bicuculline by raising neuronal excitability with iontophoretically applied glutamate. 7. On the basis of these results it is suggested that the normal subdivision of the simple cell receptive field into separate "on" and "off" regions and its directional specificity are dependent on intracortical inhibitory processes that are blocked by bicuculline. The orientational tuning of simple cells conversely appears to be largely determined by the excitatory input but normally enhanced by lateral type inhibitory processes acting in the orientation domain. 8. It also appears that the excitatory input to some complex cells is not orientation specific. This suggests that for these cells it is extremely unlikely that they receive an orientation specific excitatory input from simple cells.     

Intracortical facilitation among co-oriented,co-axially aligned simple cells in cat striate cortex

Summary Most neurons in cat striate visual cortex show inhibitory effects when moving contours are presented beyond the limits of classic receptive field regions. Facilitatory effects are also present in about 40% of simple cells. Here, we report a highly specific form of this facilitation, mediated only by neurons possessing both an orientation tuning matched to the test unit, and a receptive field position aligned with its long axis. This finding illustrates one of the intracortical interconnection schemes hypothesized by Mitchison and Crick (1982). Periodic clustering in long, intrinsic axons may signify a neuron seeking specific functional interactions like these across columnar systems in both the spatial and orientation domains.     

Development of orientation tuning in simple cells of primary visual cortex

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.     

Contrast-dependent changes in spatial frequency tuning of macaque V1 neurons: effects of a changing receptive field size

Previous studies on single neurons in primary visual cortex have reported that selectivity for orientation and spatial frequency tuning do not change with stimulus contrast. The prevailing hypothesis is that contrast scales the response magnitude but does not differentially affect particular stimuli. Models where responses are normalized over contrast to maintain constant tuning for parameters such as orientation and spatial frequency have been proposed to explain these results. However, our results indicate that a fundamental property of receptive field organization, spatial summation, is not contrast invariant. We examined the spatial frequency tuning of cells that show contrast-dependent changes in spatial summation and have found that spatial frequency selectivity also depends on stimulus contrast. These results indicate that contrast changes in the spatial frequency tuning curves result from spatial reorganization of the receptive field.     

Collinearity tolerance of cells in areas 17 and 18 of the cat's visual cortex: Relative sensitivity to straight lines and chevrons

Summary Collinearity tolerance and length dependence of orientation tuning were compared in cells recorded from areas 17 and 18 of the lightly anaesthetised cat's visual cortex. Orientation tuning and interaction between receptive field halves of the same cells are reported in the preceding paper and elsewhere (Hammond and Andrews, 1978a, b).In confirmation of previous work, increase in stimulus length was associated with sharper orientation tuning in all simple and hypercomplex cells, and in most complex cells even in the absence of length summation.Cells in areas 17 and 18 were more sharply tuned for straight lines than for chevrons bent symmetrically about the optimal orientation; tuning for chevrons was noticeably skewed compared with tuning for straight lines. In area 17, the best response was always obtained with a straight line of optimal orientation.The two halves of the receptive fields of some cells in area 18 had dissimilar preferred orientations. Even in cells whose receptive field halves were similarly tuned, broadly tuned, or apparently untuned for orientation, simultaneous stimulation of both halves of the receptive field led to substantial sharpening of tuning. In cells with dissimilarly tuned half fields, the skew in chevron tuning was predictable from the orientation tuning of each half of the receptive field. Two area 18 cells responded consistently better to a chevron stimulus than to a straight line of any orientation.     

Neurophysiological and simulation studies of striate cortex receptive field maps: The role of intracortical interneuronal interactions

Acute experiments on 27 adult anesthetized and immobilized cats investigated 101 on and off receptive fields in 67 neurons in visual cortex field 17 by mapping using single local stimuli presented sequentially at different parts of the visual field, as well as in combination with additional stimulation of the center of the receptive field. Both classical and combined mapping identified receptive fields with single receptive zones (63.4% and 29.3% respectively), along with fields consisting of several (2-5) excitatory and/or inhibitory zones (36.6% and 70.7%). We provide the first report of receptive fields with horseshoe, cross, and T shapes. Simulations of horizontal interneuronal interactions in the visual cortex responsible for the multiplicity of excitatory and inhibitory zones of receptive fields were performed. A role for cooperative interactions of neurons in this effect was demonstrated. The possible functional role of receptive fields of different types in extracting the features of visual images is discussed.     

The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat''s striate cortex

1. The GABA antagonist bicuculline has been applied to hypercomplex cells in layers II and III of the cat's striate cortex in an attempt to test the hypothesis that their length preference derives from the action of a GABA mediated post-synaptic inhibitory input.2. Iontophoretic application of bicuculline to these cells resulted in a reduction but not an elimination of the length preference. The reduction in length preference was only observed in the case of slits extended to one side of the receptive field or to slits only partially covering what appeared to be inhibitory flanking regions either side of the field centre. In cells normally showing a clear and stable length preference it was never possible to produce by the application of bicuculline a significant response to a slit fully extended to cover both flanking regions.3. The orientation tuning was basically eliminated by the application of bicuculline. In contrast the directional specificity was relatively unaffected.4. The action of bicuculline on hypercomplex cell orientation tuning supports the view that GABA mediated inhibitory inputs were effectively blocked and suggests that the partial effect on length preference and lack of effect on directional specificity reflect the varying degree of involvement of a GABA mediated inhibitory input to these receptive field properties.5. These observations introduce the possibility that the excitatory input to the superficial layer hypercomplex cells exhibits directional specificity, length preference with respect to a slit extended to both sides of the field and a low degree of orientation selectivity. Evidence is presented indicating that certain layer V cells with hypercomplex type receptive field properties exhibit some of the characteristics required of this input.     

Image features selected by neurons of the cat primary visual cortex

The sensitivity of neurons in field 17 of the visual cortex in cats to cross-shaped, Y-shaped, and star-shaped figures flashing in the receptive field was studied. About 40% of the neurons studied (114 of 289) were found to generate large responses (with an average response factor of 3.06±0.32) to one of the figures flashing in the center of the receptive field, as compared with the responses produced to a single bar in the optimal orientation. Most of these neurons (72%) were selectively sensitive to the shape and orientation of figures; the remainder demonstrated some degree of tuning invariance to these properties. The latent periods of responses to figures were usually shorter than those of responses to bars. Tuning parameters for bars and figures were generally related: neurons with acute orientational tuning to a bar were usually highly selective to both the configuration and the orientation people figures. Separate or combined stimulation with crosses in the center and near periphery of the receptive fields demonstrated summation, antagonism, or the lack of any interaction between these zones in producing sensitivity to crosses. Local blockade of intracortical GABAergic inhibition by microiontophoretic application of bicuculline showed that in one third of the neurons studied, sensitivity to figures was generated or enhanced by inhibition in normal conditions, while one third of cells showed suppression by inhibition, and sensitivity in the remainder was independent of inhibition. These data show that reconsideration of existing concepts of the role of field 17 in selecting only first-order shape features of images (i.e., the orientations of single lines) is needed, since almost half the neurons in the cat primary visual cortex can efficiently detect second-order features (angles and line intersections). Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 85, No. 6, pp. 767–780, June, 1999.     

Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects

A fundamental feature of neural circuitry in the primary visual cortex (V1) is the existence of recurrent excitatory connections between spiny neurons, recurrent inhibitory connections between smooth neurons, and local connections between excitatory and inhibitory neurons. We modeled the dynamic behavior of intermixed excitatory and inhibitory populations of cells in V1 that receive input from the classical receptive field (the receptive field center) through feedforward thalamocortical afferents, as well as input from outside the classical receptive field (the receptive field surround) via long-range intracortical connections. A counterintuitive result is that the response of oriented cells can be facilitated beyond optimal levels when the surround stimulus is cross-oriented with respect to the center and suppressed when the surround stimulus is iso-oriented. This effect is primarily due to changes in recurrent inhibition within a local circuit. Cross-oriented surround stimulation leads to a reduction of presynaptic inhibition and a supraoptimal response, whereas iso-oriented surround stimulation has the opposite effect. This mechanism is used to explain the orientation and contrast dependence of contextual interactions in primary visual cortex: responses to a center stimulus can be both strongly suppressed and supraoptimally facilitated as a function of surround orientation, and these effects diminish as stimulus contrast decreases.     

Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells

The relationship between orientation selectivity and spatial receptive field organization was analyzed. Receptive field maps were made with a dual stimulus technique where an optimally oriented activation slit was presented in the most responsive region to produce activity against which the effect of a test spot in various positions was determined. Both simple and complex cells had receptive fields which were subdivided into adjacent elongated and antagonistic subregions. When the two stimuli were presented in phase (both ON or OFF simultaneously) the fields had a central enhancement region with a strong suppression flank on one or both sides. Optimal slit orientation was related to the location of the suppression flank relative to the location of the central enhancement region, and the degree of orientation selectivity to the shape of the subregions and the distance between them. Estimated orientation tuning curves calculated from the receptive field maps gave satisfactory first approximations to experimental curves. The relative contribution of enhancement and suppression to orientation selectivity was studied by presenting a test slit in different orientations in phase with an optimally oriented activation slit. The orientation selectivity was produced almost exclusively by the flank suppression indicating that orientation selectivity is produced by inhibitory input. The flank suppression lacked any specific orientation selectivity, and it occurred only when both the central region and the flanks were activated in phase. Orientation selectivity in both simple and complex cells is explained by a receptive field organization where the cells have input from partially overlapping excitatory and inhibitory fields which have their centers slightly displaced from each other.     

Receptive fields of units in the visual cortex of the cat in the presence and absence of bodily tilt

Summary The receptive fields of units in the visual cortex of anaesthetised cats were studied using spots or slits of light. Some fields were found to be stable when they were repeatedly plotted with the cat maintained in the horizontal position: other fields were not stable and the sharpness of spatial tuning varied though the orientation of the axis did not shift. When the cat was tilted the field axis of the majority of cells followed the tilt. In 14 cells, however, changes occurred in the receptive field which were not observed when the animal remained in the horizontal plane. These changes included drifts of the field axis in a direction which, with one exception, was opposite to the tilt, and alterations in the spatial extent of the field. On returning the animal to horizontal the axis of 4 fields drifted past the original orientation. These effects were not eliminated by either bilateral destruction of the labyrinth or high cervical transection of the spinal cord. The time of onset of the tilt effects varied from cell to cell: some of this variability is probably an effect of anaesthesia.The findings are consistent with the view that the receptive field of certain cells in the visual cortex are capable of being modified, one of the modifying influences being the orientation of the body in space.This work was supported by grants from the Science Research Council to G. Horn and from the U.S. Public Health Service to G. Stechler (Grant MH 16215) and R.M. Hill (Grant NB 05653).     

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.     

Disinhibition as a Mechanism for Visual Cortex Neurons to Tune to Cross-Shaped Figures

A discrete simulation model of a receptive field selectively responding to cross-shaped figures, as seen in 40% of primary visual cortex neurons in the cat, was studied. The model was based on disinhibition of end-stop inhibition in the receptive field by the lateral disinhibition zone. These experiments showed that this mechanism can produce selective or, conversely, invariant tuning to the shape and orientation of cross-shaped figures and could underlie the high sensitivity of neurons to second-order image features.     

Cortical maps of separable tuning properties predict population responses to complex visual stimuli

In the earliest cortical stages of visual processing, a scene is represented in different functional domains selective for specific features. Maps of orientation and spatial frequency preference have been described in the primary visual cortex using simple sinusoidal grating stimuli. However, recent imaging experiments suggest that the maps of these two spatial parameters are not sufficient to describe patterns of activity in different orientation domains generated in response to complex, moving stimuli. A model of cortical organization is presented in which cortical temporal frequency tuning is superimposed on the maps of orientation and spatial frequency tuning. The maps of these three tuning properties are sufficient to describe the activity in orientation domains that have been measured in response to drifting complex images. The model also makes specific predictions about how moving images are represented in different spatial frequency domains. These results suggest that the tangential organization of primary visual cortex can be described by a set of maps of separable neuronal receptive field features including maps of orientation, spatial frequency, and temporal frequency tuning properties.     

Orientation tuning of surround suppression in lateral geniculate nucleus and primary visual cortex of cat

We previously suggested that orientation-tuned surround suppression of responses of cells in the primary visual cortex (V1) is primarily caused by a decrease in geniculocortical input for the cell [Ozeki H, Sadakane O, Akasaki T, Naito T, Shimegi S, Sato H (2004) Relationship between excitation and inhibition underlying size tuning and contextual response modulation in the cat primary visual cortex. J Neurosci 24:1428-1438]. To further test this hypothesis, we compared the strength of orientation and spatial phase selectivity of surround suppression, and the spatial extent of the extraclassical receptive field (ECRF) between the lateral geniculate nucleus (LGN) and V1 neurons of anesthetized cats. Extraclassical surround suppression in the LGN was well tuned to orientation-contrast and relative spatial phase between the classical receptive field (CRF) and ECRF stimuli. Significant orientation-tuned surround suppression was observed in 72.6% of the LGN neurons and the 66.7% of the V1 neurons tested. The degree of orientation selectivity of ECRF in LGN was comparable to that in V1; however, the strength of the relative spatial phase selectivity of ECRF in LGN was higher than that previously reported for V1 [Akasaki T, Sato H, Yoshimura Y, Ozeki H, Shimegi S (2002) Suppressive effects of receptive field surround on neuronal activity in the cat primary visual cortex. Neurosci Res 43:207-220; DeAngelis GC, Freeman RD, Ohzawa I (1994) Length and width tuning of neurons in the cat's primary visual cortex. J Neurophysiol 71:347-374]. In 70% of the LGN neurons that exhibited significant orientation-tuned extraclassical surround suppression, the effective orientation of the suppression varied according to a change in the orientation of CRF stimulus, while the remaining 30% exhibited a fixed preferred orientation of the suppression regardless of the orientation of the CRF grating. These results suggest that the basic properties of surround suppression, such as orientation and spatial phase tuning, already exist in cat LGN and that a decrease of surround suppression in excitatory inputs from LGN by surround suppression is the primary cause of surround suppression in V1. Corticogeniculate feedback may further elaborate the properties of surround suppression in LGN.