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. __________ Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 90, No. 11, pp. 1337–1347, November, 2004.     

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.     

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.     

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.     

Relationship between spatial and spatial-frequency characteristics of receptive fields of cat visual cortex

The spatial (magnitude and eccentricity) and spatial-frequency (optimum frequency and width of pass band) characteristics of the receptive fields of the cat visual cortex were investigated. It was shown that in accordance with the predictions of the theory of piecewise Fourier analysis, linear and quasilinear receptive fields of a single size comprise a modulus in each of the fields of which the index of complexity (ratio of size of field to number of periods of its optimum frequency) equals the optimum frequency multiplied by a coefficient that is constant for the given modulus. Five moduli were found with field sizes of 2.6, 3.8, 5.2, 6.2, and 7.0°, shifting with increase in the size of the modulus towards the periphery of the field of view. In accordance with predictions, when the index of complexity is fixed the width of the pass band declines inversely proportionately to the size of the fields. The obtained data directly support the hypothesis according to which the receptive fields effect a piecewise quasi-Fourier expansion of the image.Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 69, No. 5, pp. 614–622, May, 1983.     

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.     

Contextual modulation of frequency tuning of neurons in the rat auditory cortex

In a natural acoustic environment, sound stimuli often occur in a contextual acoustic stream. The aim of the present study was to determine how the frequency tuning of auditory cortical neurons is affected by an acoustic context. A forward masking paradigm was used to determine the frequency receptive fields of rat auditory cortex neurons under quiet and sequential sound conditions. The frequency receptive fields of a cortical neuron were modulated dynamically by a preceding sound stimulus. At a fixed interstimulus interval (ISI), if the preceding sound level was constant, the receptive fields of most neurons were modulated to the greatest extent when the preceding sound frequency was at or near the characteristic frequency of the neuron; if the preceding sound frequency was constant, the modulation was increased with increasing sound stimulus level. When both the frequency and the level of the preceding sound were fixed, the modulation decreased with increasing interstimulus interval. The results indicate that the frequency tuning of auditory cortical neurons is plastic and dynamically modulated in a reverberant acoustical environment, and the degree of modulation depends on both the frequency tuning of the neuron and the contextual acoustical stream.     

Neuronal responses from beyond the classic receptive field in V1 of alert monkeys

Responses of primary visual cortex (V1) neurons to stimuli inside the classic receptive field (CRF) can be modulated by stimuli outside the CRF. We recently reported that responses of most V1 neurons to a line in the CRF center are inhibited by large surround-stimuli and that this modulation is stimulus selective. Here we report that a significant proportion of V1 neurons in alert monkeys respond directly to stimuli outside the CRF with very long latency and much reduced selectivity. When surround stimuli are presented alone, three response patterns can be distinguished in 153 single- or multiunits tested: (1) 31.4% have no significant response; (2) 50.3% show excitatory responses that are significantly higher than spontaneous activity. The average latency of these responses is about 145 ms, 2–3 times longer than center responses; (3) 18.3% show suppressed spontaneous activity after stimulus onset. The direct surround responses are found to be only weakly selective for the orientation of contextual lines, and not selective for other contextual patterns tested. While the outburst of responses to stimuli within the CRF is not affected by reducing stimulus duration from 500 ms to 50 ms, late excitatory surround responses are virtually eliminated. We propose that the late excitatory surround responses to extra-CRF stimulation alone are the reflection of feedback from higher cortical areas and may contribute to reduced contextual inhibition of cells in V1. This could play a role in figure-ground segregation. Electronic Publication     

Responses of infragranular neurons in the rat primary somatosensory cortex to forepaw and hindpaw tactile stimuli

Infragranular layers constitute the main output of the primary somatosensory cortex and represent an important stage of cortico-cortical and cortico-subcortical integration. We have previously used chronic multiple single-unit recordings to study the spatiotemporal structure of tactile responses of infragranular neurons within the forepaw cortical representation in rats [Tutunculer B, Foffani G, Himes BT, Moxon KA (2006) Structure of the excitatory receptive fields of infragranular forelimb neurons in the rat primary somatosensory cortex responding to touch. Cereb Cortex 16:791-810]. Here we extend our understanding of this structure by studying the overlap between the forepaw and hindpaw cortical representations. We recorded 204 responsive neurons in chronic experiments from eight anesthetized rats. Overall, only 23% of neurons responded exclusively to one paw, 52% of neurons responded to two paws, 19% of neurons responded to three paws, and 5% of neurons responded to all four paws. Quantitative measures of response magnitudes and latencies revealed the following main results. (1) The responses of forepaw neurons overall displayed greater magnitudes and shorter latencies than the responses of hindpaw neurons. (2) The responses to ipsilateral stimuli displayed smaller magnitudes, and longer-and more variable-latencies than the responses to contralateral stimuli. (3) The responses of forepaw neurons to hindpaw stimuli displayed smaller magnitudes and longer latencies than the responses to forepaw stimuli, whereas the responses of hindpaw neurons to forepaw stimuli displayed smaller magnitudes but similar latencies compared with the responses to hindpaw stimuli. These results show that the spatiotemporal structure of tactile responses of infragranular neurons extends across all four paws, and provide the basic architecture for studying physiological integration and pathophysiological reorganization of tactile information in the infragranular layers of the rat primary somatosensory cortex.     

The Sensitivity of Neurons in the Lateral Geniculate Body of the Cat to the Orientation Vectors of Brightness Gradients

We describe here a new property of visual neurons: sensitivity to the magnitude and orientation of the brightness gradient vector in a test stimulus presented in the receptive field of the neuron. The brightness gradient test image was a spot (diameter 4°) on the dark background of the slide. Brightness changed linearly within the spot. The absolute value of the brightness gradient varied over the range 0.4–2.7 cd/m²/° in the direction of the brightness gradient. The integral brightness in the test spot containing the gradient image was identical for different values of the brightness gradient. The numbers of spikes in the on- and off-responses of on and off neurons in the lateral geniculate body of cats depended on the orientation of the brightness gradient vector in the test stimulus. The sensitivity of neurons to the orientation of the brightness gradient vector, K (the coefficient of sensitivity), was assessed as the normalized difference between the number of spikes in neuron responses in the preferred and non-preferred orientations of the brightness gradient vector in the neuron's receptive field. The mean sensitivity coefficient for 53 cells was 0.55 ± 0.20. A 6.7-fold decrease in the brightness gradient resulted in a 3.7-fold decrease in the coefficient of sensitivity (for the preferred direction of the orientation of the gradient vector); there was no change in the latent period of responses. The preferred orientation of the brightness gradient vector in the receptive fields of neurons coincided (to within ±22.5°) with the radial direction on the map of the field of vision in 45% of cases, and with the tangential direction in 26% of cells.     

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 effects of aging on the strength of surround suppression of receptive field of V1 cells in monkeys

The surround suppression of the receptive field is important for basic visual information processing, such as orientation specificity. To date, the effects of aging on the strength of surround suppression are not clear. To address this issue, we carried out extracellular single-unit studies of the receptive field properties of cells in the primary visual cortex (area V1) in young and old rhesus (Macaca mulatta) monkeys. When presented with the oriented central stimulus, we found that cells in old animals showed reduced orientation and direction selectivity compared with those in young animals. When presented with the oriented central stimulus together with the optimal surround stimulus, more selective cells {orientation bias (OB) ≥0.1; a bias of 0.1 is significant at the P<0.005 level} in animals of both ages showed reduced orientation selectivity compared with the experiment that presented only the oriented central stimulus. When presented with the optimal central stimulus together with the oriented surround stimulus, cells in old animals showed reduced orientation and direction selectivity compared with young animals. Moreover, broadly tuned cells (OB<0.1) in old animals exhibited significantly reduced suppression indices that quantified the strength of the surround suppression of the receptive field, when compared with those in young animals. These results suggest that aging may seriously affect the surround suppression of the receptive field of V1 cells. Thus, the decreased strength of surround suppression of the receptive field may be one possible reason for the decreased stimulus selectivity of V1 cells previously found in the senescent brain. This work will contribute to an understanding of the physiological mechanisms mediating surround suppression of the receptive field.     

Mechanisms of binocular interaction in the visual cortex of rodents

New hypotheses are advanced relating to the functional role and mechanisms of interaction of afferentation from the two eyes in the visual cortex of animals with poorly developed binocular vision. The proposed approach sheds light on a number of questions, particularly those concerning the relatively large level of disparity of the receptor fields in cortical neurons, the role of non-overlapping fibers in the visual tract, and others. Hypothesis relating to the evolutionary relationships between these mechanisms and the mechanisms of stereopsis are discussed. A. B. Kogan Science Research Institute of Neurocybernetics, Rostov State University, Rostov-on-Don. Translated from Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 81, No. 5, pp. 31–39, May, 1995.     

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. __________ Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 92, No. 2, pp. 152–163, February, 2006.     

Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast

Summary Extracellular responses of single units in striate cortex of the cat were studied quantitatively. Sinusoidal gratings were used as stimuli and the variables of interest were orientation and contrast. Specifically, we wanted to determine if orientation tuning was dependent on contrast. Of 45 cells studied in detail, two basic types of contrast-response pattern were observed, but most patterns were intermediate between these extremes. In one type, responses increased approximately linearly with log contrast while in the second, saturation was found at low contrast levels. For all these cells, orientation tuning characteristics were independent of contrast. An additional observation, made from 14 cells, was that stimuli presented at non-optimal orientations can suppress responses to below the general maintained discharge levels. In eight of these cases, the inhibition was clearly contrast-dependent.Supported by US National Institutes of Health Grant EY01175 and Research Career Development Award EY00092 to R.D. Freeman. G. Sclar received support from National Institutes of Health Training Grant EY07043     

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

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

Neurophysiological Correlates of Delayed Visual Differentiation Tasks in Monkeys: the Effects of the Site of Intracortical Blockade of NMDA Receptors

A delayed visual differentiation task using stimuli of different colors was used in rhesus macaques to study the characteristics of visual recognition, short-term memory, and the responses of neurons recorded simultaneously in the visual and prefrontal areas of the cortex, along with their relationships with the site of intracortical (fields 17 or 46) perfusion of the glutamate receptor antagonist 2-amino-5-phosphonovaleric acid (APV). The behavioral characteristics and spike activity of individual cells in cortical fields 17 and 46 were recorded before and after perfusion with APV and after washing away of traces of APV. Multifactor dispersion analysis showed that the effect of APV in monkeys consisted of decreases in the probability of correct responses, leading to a decrease (two-fold) in the duration of short-term storage of information and a significant increase in the motor reaction time. The probability of correct solutions depended on the site of APV perfusion in the cortex, while the motor response time was independent of the perfusion site. Perfusion of field 46 with APV, unlike perfusion of field 17, altered the spike activity only of neurons in the prefrontal cortex, while no significant changes were seen in the neuron activity of the visual cortex. The actions of APV were accompanied by significant desynchronization of neuron activity in these two areas as compared with the level of synchronization in normal conditions; after traces of APV were washed away, the extent of desynchronization decreased. The neurophysiological correlates of cognitive dysfunctions associated with degradation of visual recognition and short-term memory due to modification of glutamatergic structures by blockade of NMDA receptors are discussed.     

Structural changes in visual cortex area 17 in children with aftereffects of perinatal injury to the central nervous system

Structural characteristics of the visual cortex area 17 were studied by computer morphometry on autopsied specimens of the brain from children with perinatal injury to the central nervous system and in a group of control children without symptoms of brain injury. In children with perinatal pathology, the thickness of the cortex and its individual layers (IV, V, VI+VII) increased unevenly during the 1st year of life, the density of neurons decreased, while the content of neuroglia increased. These disorders reflect nonspecific structural and functional changes in the visual cortex associated with perinatal cerebral pathology. __________ Translated from Byulleten’ Eksperimental’noi Biologii i Meditsiny, Vol. 143, No. 6, pp. 700–703, June, 2007