I. A. Shevelev

Tuning of striate neurons to cross-shaped figures in conditions of local blockade of intracortical inhibition

The recently observed selective sensitivity to cross-shaped and angular figures was studied in 85 primary visual cortex (field 17) neurons in cats before and after local blockade of GABAA ergic inhibition by microiontophoretic application of the GABA antagonist bicuculline. Two opposite effects were seen: half of the neurons studied showed decreases or complete loss of sensitivity to crosses, and a third of the cells showed increases or the appearance of sensitivity to crosses. These data provide evidence for significant roles for intracortical inhibition in providing sensitivity to crosses and intersecting lines in two types of visual cortex neurons, the effects on these two types of neuron being opposite.

A model of a neuronal network for detection of single bands and cross-like figures.

A model of a neuronal network is presented which, like a significant proportion of the neurons in the visual cortex, identifies not only the orientation of a single band, but also high selective sensitivity to cross-like figures. The model was used to study the properties of a “cross detector” constructed on the basis of convergence of excitatory connections with different weightings from elements with different orientational tuning. It is shown that a cross detector with monomodal orientational tuning needs an amplifier mechanism (a reverberator).

Characteristics of the responses of visual cortex neurons with sensitivity to bars or cross-shaped figures in cats.

The magnitudes and latent periods of spike responses were recorded from 280 individual neurons tuned to the orientation of light bars or cross-shaped figures in the primary visual cortex (field 17) of the cat. In control experimental conditions, half of 195 cells preferred the bar (first group), the remainder preferring crosses (second group); the responses of neurons of the first group to bars and crosses were of similar magnitude, while in the second group, responses to crosses were significantly larger than responses to bars. The latent periods of responses to optimal bars in the first group of neurons were shorter than those in the second group, and became longer on exposure to crosses, while latent periods in the second group were shorter on exposure to crosses. In conditions of local bicuculline blockade of intracortical inhibition, about a quarter of 85 neurons were sensitive only to the bar, regardless of the presence or absence of inhibition. The remaining neurons were sensitive to crosses in at least one of the states and continued to have responses which were smaller in terms of absolute magnitude than the responses of group 1 neurons. The significance of these data for understanding the mechanisms of tuning of striate neurons to signal features and the temporal sequence of their operation is discussed.

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.

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.

The Time Course of Disinhibition of Visual Cortex Neurons and Sensitivity to Cross-Shaped Figures

The relationship between the responses of 74 neurons in field 17 of the cat cortex to presentation of cross-shaped figures flashing in their receptive fields and the asynchronicity with which the lines of the figures were presented were investigated. The cross sensitivity of neurons was studied with simultaneous, leading, and delayed activation of the disinhibitory zone of the receptive field in relation to the time at which its major excitatory and end-stopping inhibitory zones were stimulated. Two types of temporal interaction were identified between the receptive field zones determining cross sensitivity. In cells of the first type (14 of 23 cells), the response was maximal in conditions of simultaneous stimulation of the major and disinhibitory zones of the receptive field; neurons of the second type (nine of 23 cells) showed the opposite temporal relationship. Digital simulation showed that cross sensitivity in neurons of the first type was supported by disinhibition of end-stopping inhibition, while in neurons of the second type it depended on a combination of disinhibitory and convergence mechanisms.

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.

The Disinhibitory Zone of the Striate Neuron Receptive Field and Its Sensitivity to Cross-Like Figures

Acute experiments on immobilized anesthetized cats were used to confirm the suggestion that the sensitivity of many neurons on the primary visual cortex to cross-shaped, angular, and Y-shaped figures may be determined by the presence within their receptive fields of disinhibitory zones, which block end-stopping inhibition. A total of 55 neurons (84 functions, i.e., on and off responses) were used for studies of sensitivity to crosses, and responses to single bars of different lengths were compared before and after stimulation of an additional lateral zone of the field (the presumptive disinhibitory zone), which was located in terms of responses to crosses. Seventeen of the 55 cells in which increases in the length of a single bar decreased responses, i.e., which demonstrated end-stopping inhibition, showed significant increases in responses (by an average factor of 2.06 ± 0.16) during simultaneous stimulation of the lateral zone of the receptive field, which we interpreted as a disinhibitory effect on end-stopping inhibition. These data provide the first direct evidence for the role of end-stopping inhibition and its blockade by the disinhibitory zone of the receptive field in determining the sensitivity of some neurons in the primary visual cortex of the cat to cross-shaped figures.

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.

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.