Length Summation Research Articles

The length summation properties of layer VI cells in the visual cortex and hypercomplex cell end zone inhibition

Layer VI of the visual cortex has been considered to be dominated by cells with very long receptive fields, typically summing to 8 degrees or more. We have re-examined this issue in a series of experiments in which the length tuning profiles of layer VI cells in the cat visual cortex have been quantitatively determined. Responses were assessed to optimally oriented bars of light of varying length drifted over the receptive field. The lengths were varied on a randomised interleaved sequence. Although our data confirm the presence of long field cells in layer VI, only 24% of a population of 119 cells had fields greater than 6 degrees in length. Fields greater than 8 degrees were only seen in 17% of cells. 61% of the population of cells had fields showing summation to 4 degrees or less with a mean length of 2.8 degrees (+/-0.15 sem). In this "short field" group, 18% had fields of 1 degrees or less. We observed 7 cells with rapid initial spatial summation up to 1 degree, followed by clear end zone inhibition. It has been recently suggested on the basis of localised inactivation experiments, that layer VI cells with long (greater than 8 degrees) fields may provide the drive to inhibitory interneurones in layer IV generating hypercomplex cell end zone inhibition. This observation is difficult to equate with evidence indicating that hypercomplex cell end zone inhibition reflects a mechanism showing maximal summation at lengths in the region of 2.8 degrees.(ABSTRACT TRUNCATED AT 250 WORDS)

Modulatory influences of a moving visual noise background on bar-evoked responses of cells in area 18 of the feline visual cortex

The modulatory influence of a synchronously moving visual noise background on responsiveness to an optimally-oriented moving bar stimulus was investigated in visual cortical area 18 of the lightly-anaesthetized cat. The bar and noise background were swept along the axis orthogonal to bar orientation, with the same phase, velocity and amplitude of motion. Cells which were insensitive to motion of visual noise per se or weakly responsive to individual 'grains' in the noise sample showed suppression of bar-evoked responses by simultaneous motion of the noise background. Percent suppression declined with increase in bar length, over a range which could exceed the maximum estimate of receptive field length. The decline in percent suppression was non-linear, becoming progressively flatter in slope as bar length was increased until an asymptotic value was reached; observations on end-stopped cells and on end-free cells with restricted length summation verified that percent suppression was related specifically to the length of the comparison bar and not to the strength of response it evoked. Percent suppression and the extent over which it declined with increase in bar length were comparable for preferred and opposite directions of bar motion even in cells with radically different length-response functions in the two directions, including end-stopped cells with direction-selective end-zones. In contrast to end-inhibition, which was maximal at or near the preferred velocity for a bar of optimal length, percent suppression by motion of the noise background was essentially velocity-invariant; in velocity tuned and velocity high-pass cells, background motion reduced the slope(s) of the velocity-response function, implying that the suppressive action of moving noise backgrounds is divisive rather than subtractive. It is argued that the suppression derives predominantly from an axo-somatic noise-sensitive inhibitory input from superficial- and deep-layer, large basket cells in orientation 'columns' at some distance from those of their target cells.

Areal influences on complex cells in cat striate cortex: stimulus-specificity of width and length summation

In single neurones recorded from the striate cortex of cats anaesthetized with N2O/O2/halothane, receptive field dimensions, length specificity and areal extent of drive were assessed for different classes of visual stimuli. Receptive fields were mapped as rectangular minimum response fields (MRFs). Spatial summation along the axis of preferred orientation was assessed: for moving bars whose length was varied (length summation); and for height variation of a square-wave grating patch against a uniform grey background, or a patch of moving texture against a stationary background of similar texture. In complementary tests a moving square-wave grating background was progressively occluded by a uniform grey foreground mask of variable height; or a mask of stationary texture of variable height progressively occluded a background of moving texture. In parallel measurements, the width of grating or textured patches or masks was varied whilst maintaining height constant. Broadly speaking, the areal influence of each class of stimulus was comparable, and distinct from extra-receptive field phenomena in evoking responses from within the receptive field, but not from surrounding areas. The masking paradigm provided the most sensitive measure of receptive field height and width. However, in some neurones length summation, the degree of end-stopping, and the directional bias depended critically on the stimulus configuration used. Length summation tended to be more dramatic for short bars than for gratings. Length summation for texture was significantly more pronounced than for an oriented bar in special and in intermediate complex neurones. By contrast, endstopping was typically less intense for gratings than for bars, and least pronounced for texture. Because of stimulus specificity, complex neurones assigned to particular functional subgroups on the basis of their response to oriented bars may exhibit quite different patterns of behaviour for other classes of stimuli.

The influence of stimulus length on the oblique effect of contrast sensitivity

Contrast sensitivity for gratings of different orientations was measured at various stimulus lengths. The oblique effect of contrast sensitivity was observed to increase in magnitude as the length of the truncated gratings was increased from 0.5 to 5.6deg. This finding refutes a purported distinction between the contrast sensitivity oblique effect and the orientation discrimination oblique effect. Thus, these results are consistent with the idea that the contrast sensitivity oblique effect and the orientation discrimination oblique effect share the same common underlying anisotropic basis. These results also show that grating summation differs at oblique and nonoblique orientations in terms of length summation as well as in terms of width summation.

Physiological, morphological, and cytochemical characteristics of a layer 1 neuron in cat striate cortex.

We have recorded from a small neuron in layer 1 of the striate visual cortex in a 34-day-old kitten. It had a simple, orientation-selective receptive field that was nondirectional and showed length summation. The neuron was injected intracellularly with horseradish peroxidase. Computer-aided reconstruction revealed that it had a dense axonal plexus confined to layer 1, elongated in the anteroposterior dimension. By means of an antibody directed against a GABA-like antigen, and postembedding immunocytohemistry, the neuron was found to be strongly immunoreactive. The main input to soma and dendrites of the neuron was from synapses that were not GABA-L-immunoreactive, and probably originated from pyramidal cells. The axon of the cell formed synapses on dendritic shafts and spines, whose most likely sources were the apical tufts of pyramidal cell dendrites. These data suggest that such neurons may be involved in local circuits that contribute to the formation of pyramidal cell receptive fields.

Vernier acuities of neurons in area 17 of cat visual cortex: Their relation to stimulus length and velocity, orientation selectivity, and receptive-field structure

The sensitivity of neurons in area 17 of the cat's visual cortex to vernier offset was expressed as the percentage reduction in response caused by the introduction of a given offset into a bar stimulus moving across the receptive field. There was a wide variation in sensitivity: in some cells response could be halved by an offset equal to a fifth receptive-field width (defined as twice the standard deviation of a Gaussian curve fitted to the response profile), while other cells showed no sensitivity. The highest absolute sensitivities of complex and simple cells were similar, although most cells with poor sensitivity were complex. Sensitivity was largely unaffected by changes in stimulus velocity and stimulus length, although there was a tendency for sensitivity to increase with decreasing bar length. Comparisons of orientation tuning curves with vernier tuning curves showed that the response to a vernier stimulus approximated the response to a single bar of the same overall length and an orientation equal to that of a line joining the midpoints of each bar. This was true for a wide range of sensitivity values. Vernier sensitivity was correlated with a measure of length summation H, which is positive when there is net facilitation between the bars, and negative when there is net inhibition. Vernier sensitivity was highest in cells with large values of H, and least in cells where H was negative. We examined a linear model of the simple cell receptive field which, together with a variable response threshold, was able to explain the correlation between vernier acuity and length summation. Although this model accounted qualitatively for many of our findings, the majority of simple cells had tuning curves that were sharper than the predicted ones. This suggests that there are nonlinearities in the behavior of many simple cells whose effect is to increase the sharpness of orientation tuning and consequently vernier sensitivity.

Directional and orientational tuning of feline striate cortical neurones: Correlation with neuronal class

In a subset of 327 simple and complex cells from the striate cortex of cats anaesthetized with N 2O/O 2/halothane, a range of receptive field properties were compared. These included directional and orientational selectivity, tuning and symmetry; endstopping; receptive field dimensions; length summation; texture sensitivity; ocular dominance; and resting discharge levels. These properties were related to neuronal class (simple or complex) and to the special, intermediate and standard subdivisions of the complex cell category. Special complex cells showed a high incidence of direction selectivity, were less sharply tuned for orientation, more commonly endstopped, more strongly binocular, tended to have higher resting discharge levels and exhibited greater sensitivity to motion of randomly textured patterns than the other classes of neurones. The remaining classes of complex cells, together with simple cells, were more commonly direction-biased or bidirectional, and more selective for orientation than special complex cells. Standard complex cells were marginally more symmetrically tuned for orientation than the other groups. Simple cells represented the most sharply orientation tuned neurones in the cortex; unlike complex cells of all groups they were insensitive to texture motion, generally had lower levels of maintained discharge, and showed least integration of inputs between the two eyes. Assessed by appropriate measures (minimum response fields in special complex cells; length summation in standard complex cells), standard complex cells had significantly larger receptive fields than special complex cells.

Cat area 17. III. Response properties and orientation anisotropies of corticotectal cells.

The receptive field properties of antidromically identified corticotectal (CT) cells in area 17 were explored in the paralyzed, anesthetized cat. To compare these with another population of infragranular cells, we also examined the receptive field properties of cells in layer 6. Sixty percent of our sample of CT cells showed increased response to increased stimulus length (length summation) and were classified as standard complex cells. The other 40% showed little or no length summation, were generally end stopped, and were classified as special complex cells. Standard and special complex CT cells have complementary orientation anisotropies: the distribution of orientation preferences of standard complex cells is biased toward obliquely oriented stimuli, whereas special complex cells are biased toward horizontally and vertically oriented stimuli. The receptive fields of the cells in our sample were primarily along the horizontal meridian so we cannot determine if these anisotropies are defined relative to the vertical meridian or relative to the meridian passing through the receptive field. The effects of these anisotropies in preferred orientation are minimized by the broad orientation tuning of CT cells. There was no simple relationship between the direction bias of CT cells and the reported direction bias of tectal cells. In contrast to the heterogeneity of corticotectal cells, layer 6 cells uniformly showed strong length summation, tight orientation tuning, and little spontaneous activity.

Length summation of complex cells in cat striate cortex: A reappraisal of the “special/standard” classification

A reappraisal of the relationship between length summation and receptive field length assessed by the minimum response field method, was made in complex cells recorded from the lightly anaesthetized feline striate cortex. This relationship has previously been proposed by Gilbert [(1977) J. Physiol., Lond. 268, 391–421 and subsequently applied extensively by others, as a basis for subdividing complex cells into different functional groups: “standard” complex cells length summate, responding preferentially to long contours of appropriate orientation; “special” complex cells respond optimally to short oriented contours). Quantitative comparisons suggest that four-fifths of complex cells can be classified by their length summatory behaviour. Thus length summatory behaviour is a useful adjunct to classification, although one-in-five complex cells cannot be positively assigned to either category and this figure rises to one-in-three following rigid application of the criteria for determining standard complex cells. The need for precise estimates of length summation is emphasized by subjective assessment which leads to greater uncertainty in classification and to several cells being wrongly assigned. The possibility that cells unclassified by length summation constitute a distinct additional class is discussed.

Influence of luminance gradient reversal on complex cells in feline striate cortex.

The effects of reversing the polarity of luminance contrast in adjacent segments of a bar stimulus have been investigated in complex cells of area 17 in cats lightly anaesthetized with nitrous oxide/oxygen halothane mixtures. On the basis of length summation behaviour, complex cells were classified as standard (length summating) or special (optimum response to a bar much shorter than the receptive field), after Gilbert (1977), and were further subdivided into groups lacking and possessing end-stopping. For each type of complex cell, we measured the effects of adding short segments of one polarity of contrast (light or dark) to either end of a bar of fixed length and optimum orientation but of opposite contrast. In all cells the response to the central bar was depressed by short segments of reversed contrast to an extent greater than predicted from the cells' length summation characteristics. Responses were minimized or abolished at a critical segment length. Increases beyond the critical length elicited a progressive recovery in response to a plateau level. In end-stopped cells this was followed by a further decline in response up to the limits of the cells' inhibitory end-zones. Special and standard complex cells differed only in their susceptibility to reversed-contrast segments above the critical length. In standard complex cells, the recovery of response matched the cells' length summation profiles in slope and cut-off point. In special complex cells the recovery was flatter in slope and significantly more protracted than the length summation profile. Similar results were obtained for either direction of motion (orthogonal to a cell's optimum orientation) and for either polarity of contrast (dark centre, light ends or the reverse). As might be expected, all the effects were weighted in favour of the receptive field centre. Thus the upturn in response as reversed-contrast segments were progressively extended was more rapid and achieved a higher limiting level when the central bar was short. Merely interrupting the contours of a bar by a central gap, rather than a segment of reversed contrast, gave rise to no more attenuation of response than that predictable from the length summation curve. The results are compared and contrasted with our comparable data for simple cells.

Spatial summation in subregions of simple-cell receptive fields in cat striate cortex as a function of slit length.

Spatial summation along the optimum stimulus orientation in subregions of simple-cell receptive fields in cat striate cortex was studied quantitatively by measuring the response to stationary light slits of variable length. Before summation analysis, the cell's discharge field was mapped by flashing a test slit on and off in a sequence of positions through the receptive field. A static activation procedure was used to determine the extension of subregions of the receptive field where light stimulation increased (enhancement) or decreased (suppression) the firing rate. An activation slit in the optimum orientation was positioned in the most responsive position of the discharge field and the effects of a parallel test slit, in a series of broadside positions, were assessed from the changes induced in the discharge elicited by the activation slit. Length-response curves for on and off responses were made by positioning a test slit in the respective subregions of the discharge field. The activation procedure was used to make length-response curves for suppression. A test slit of variable length was positioned in a suppression region defined by the activation profiles and an activation slit of fixed length was centred in the most responsive discharge field position. Length summation was found for all cells, both with respect to on and off responses, and suppression. The curves for on and off responses had a maximum value beyond which the response declined or levelled off, but some cells had a secondary, more shallow increase beyond an initial, steeply rising part. Similar properties were found for summation of suppression except that the effects were opposite in sign. Curves made for both on and off regions in the same cell often differed in shape. Such differences were also found when length-response curves made in different suppression regions of the same cell were compared. The various length-summation functions were explained by a model presuming that simple-cell receptive fields consist of partially overlapping non-concentric excitatory and inhibitory fields. This arrangement would also explain why length-response curves in various subregions often had different shapes.

Length summation in simple cells of cat striate cortex.

We have examined two models for the preference displayed by cortical simple cells for elongated stimuli having a particular orientation. Both assume that geniculate afferents with aligned receptive fields pool to form the receptive field of the cortical unit. The first model [Marr and Hildreth, Proc. R. Soc. Lond. Ser. B 200, 269-294 (1980)], includes AND gating along the length axis so that a simple cell does not fire unless a critical number of its afferents with adjacent receptive fields are firing. The second model assumes that geniculate input is simply summed over subunits and then passed through a firing threshold. Both models account for the unresponsiveness of simple cells to spots of light, but the AND model predicts a discontinuous length threshold, while the summation model predicts that length and contrast should be interchangeable in the determination of the response threshold. Experiments in which length and contrast were systematically varied support the summation model, and extend the notion of linear spatial summation to the length axis in simple cells.

Contribution of the cortico-claustral loop to receptive field properties in area 17 of the cat

The contribution of the cat's claustrum to the response properties of cells in area 17 was studied by destroying the left claustrum and examining receptive field properties of cells in both the left and right area 17. For each cell we assessed sharpness of orientation tuning, degree of direction selectivity, length summation, end-stopping, ocular dominance, responsiveness, and several other properties. On the lesioned side, 462 cells were studied, and on the control side, 636 cells. All cats showed a reduction in the number of end-stopped cells in area 17 on the side of the lesion. This was particularly marked in layers 2 + 3 and 4, where end-stopped cells are normally most abundant. In the control hemisphere, 43% of the sample from these layers showed at least moderate end-stopping whereas, in contrast, only 21% exhibited this degree of end-stopping on the side of the lesion. There was no obvious change in other response properties. We conclude that one function of the cat's claustrum is to help regulate the length selectivity of cells in area 17.

Influence of luminance gradient reversal on simple cells in feline striate cortex.

1. The sensitivity of simple cells to luminance gradient reversal in bar stimuli has been investigated in the striate cortex of lightly anaesthetized cats.2. The influence of segment(s) of one polarity of contrast, partially masking or added end-on to a bar of reversed contrast, was assessed against a stationary textured background (of intermediate average luminance), which was itself without influence on cell behaviour.3. In either configuration, short segments of reversed contrast were suppressive of bar response, to an extent varying with location along the receptive-field axis, but much greater than predictable from length-summation characteristics. Response suppression, even by very short segments, was often total.4. The effects of longer segments, added end-on to a bar of opposite contrast, depended on the extent of length summation exhibited by each cell. With progressive extension of these segments, some recovery of response occurred in a few simple cells with larger receptive fields, but not in small-field simple cells. The behaviour of end-stopped simple cells was comparable in all respects to that of their end-free counterparts, within the length-summation zone; thereafter, invasion of the inhibitory end-zones by bars of either polarity elicited a generalized decline in response.5. Where responsiveness was restored by adding longer segments of opposite polarity, the response peak shifted to the discharge centre appropriate to that polarity.6. All these results were found with either polarity of contrast, i.e. a light bar plus dark segments or the converse.7. Similar results were obtained for motion in either direction across the receptive field; and also for flash-presentation, over either the centre or flanks (whether ;on' or ;off') of the receptive field.8. The effectiveness of contrasting added segments was assessed as a function of location along the receptive-field axis for flash-presented and for moving stimuli. Suppressive effects were greatest over the centre of the receptive field, declining progressively in either direction along its axis, but over greater distances than anticipated from length summation.9. None of the results presented could have been predicted from length-summation characteristics. They are strongly suggestive of gating, rather than linear, antagonistic interactions.

Effects of luminance gradient reversal on complex cells in cat striate cortex.

We have examined the responsiveness of various classes of complex cells in the cat's striate cortex to stimuli comprising bars aligned with segments of opposite luminance contrast. In all cases, a short segment of opposite polarity depressed, without abolishing, the bar response; within the length summation zone, the response to the bar in the presence of longer segments matched the length summation characteristics of each cell, depressed by a constant amount. The results could not be accounted for purely on the basis of convergent input from simple cells, whose behaviour to comparable stimuli has previously been reported (Hammond and MacKay 1981a).

Spatial summation of responses in receptive fields of single cells in cat striate cortex.

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 degrees. 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 apporximately linear. Spatial summation of responses does not appear to be a useful characteristic for distinguishing one striate cell type from another.

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

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 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.